and Jennifer R. Sheltoncaram/PDFs/1998_Caramazza_Shelton.pdf · Domain-Speci” c Knowledge Systems...

34
Domain-Speci c Knowledge Systems in the Brain: The Animate-Inanimate Distinction Alfonso Caramazza and Jennifer R. Shelton Harvard University Abstract We claim that the animate and inanimate conceptual cate- gories represent evolutionarily adapted domain-speci c knowl- edge systems that are subserved by distinct neural mechanisms, thereby allowing for their selective impairment in conditions of brain damage. On this view, (some of) the category-speci c de cits that have recently been reported in the cognitive neuropsychological literature—for example, the selective dam- age or sparing of knowledge about animals—are truly categori- cal effects. Here, we articulate and defend this thesis against the dominant, reductionist theory of category-speci c de cits, which holds that the categorical nature of the de cits is the result of selective damage to noncategorically organized visual or functional semantic subsystems. On the latter view, the sensory/functional dimension provides the fundamental organ- izing principle of the semantic system. Since, according to the latter theory, sensory and functional properties are differen- tially important in determining the meaning of the members of different semantic categories, selective damage to the visual or the functional semantic subsystem will result in a category- like de cit. A review of the literature and the results of a new case of category-speci c de cit will show that the domain- speci c knowledge framework provides a better account of category-speci c de cits than the sensory/functional dichot- omy theory. INTRODUCTION How is conceptual knowledge organized in the brain? Evidence relevant to this issue is provided by the pat- terns of semantic processing de cits in brain-damaged subjects, especially those de cits that seem to selectively affect one or another semantic category. The rst clear demonstration of a semantic category-speci c de cit was made by Warrington and Shallice (1984). They re- ported four patients recovering from herpes simplex encephalitis who were disproportionately impaired in producing and understanding the names of living things. This result, coupled with the observation of a brain-dam- aged subject who showed the reverse dissociation—that is, relative sparing of the comprehension of living rela- tive to nonliving things 1 (Warrington & McCarthy, 1983)—invited the inference that brain damage could result in category-speci c semantic de cits. 2 Although the four cases described by Warrington and Shallice (1984) were not all tested with the same tasks or the same materials, they all showed poorer perfor- mance in producing and/or comprehending the names of living as opposed to nonliving things. In some cases the contrast in performance was quite striking: J.B.R. was only able to recognize or name 2 of 48 living things (animals or plants) but accurately described or named 45 of 48 nonliving things; similarly, S.B.Y. failed to iden- tify any of the living items but correctly identi ed 36 of 48 nonliving things. For example, J.B.R. de ned briefcase © 1998 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 10:1, pp. 1–34 as “small case used by students to carry papers” but responded “don’t know” to the word parrot; similarly, S.B.Y. de ned towel as “material used to dry people” but responded “bird that ies” to the word wasp. The other two cases reported by Warrington and Shallice, K.B. and I.N.G., could not be tested with the de nition produc- tion tasks because of their severe language production de cits, but their performance in word/picture matching tasks was poorer for animals than for nonliving things. Thus, all four cases showed disproportionate dif culty for living than for nonliving things. Con rmation of the dissociation of performance for living and nonliving things was soon obtained in many other studies of brain-damaged subjects of various etiolo- gies, including other cases of herpes simplex encephali- tis, trauma, cerebro-vascular accident, and neurosurgery (Basso, Capitani, & Laiacona, 1988; Damasio, Grabowski, Tranel, Hichwa, & Damasio, 1996; De Renzi & Lucchelli, 1994; Farah, Hammond, Mehta, & Radcliff, 1989; Farah, McMullen, & Meyer, 1991; Hart & Gordon, 1992; Hillis & Caramazza, 1991; Laiacona, Barbarotto, & Capitani, 1993; Laiacona, Capitani, & Barbarotto, 1997; McCarthy & War- rington, 1988; Pietrini, Nertempi, Vaglia, Revello, Pinna, & Ferro-Milone, 1988; Powell & Davidoff, 1995; Sartori & Job, 1988; Sheridan & Humphreys, 1993; Silveri & Gai- notti, 1988; Sirigu, Duhamel, & Poncet, 1991). And there have also been several reports documenting the reverse pattern of dissociations—that is, cases of impaired per- formance in naming and/or recognizing nonliving ob-

Transcript of and Jennifer R. Sheltoncaram/PDFs/1998_Caramazza_Shelton.pdf · Domain-Speci” c Knowledge Systems...

Domain-Specic Knowledge Systems in theBrain The Animate-Inanimate Distinction

Alfonso Caramazza and Jennifer R SheltonHarvard University

Abstract

We claim that the animate and inanimate conceptual cate-gories represent evolutionarily adapted domain-specic knowl-edge systems that are subserved by distinct neural mechanismsthereby allowing for their selective impairment in conditionsof brain damage On this view (some of) the category-specicdecits that have recently been reported in the cognitiveneuropsychological literaturemdashfor example the selective dam-age or sparing of knowledge about animalsmdashare truly categori-cal effects Here we articulate and defend this thesis againstthe dominant reductionist theory of category-specic decitswhich holds that the categorical nature of the decits is theresult of selective damage to noncategorically organized visual

or functional semantic subsystems On the latter view thesensoryfunctional dimension provides the fundamental organ-izing principle of the semantic system Since according to thelatter theory sensory and functional properties are differen-tially important in determining the meaning of the membersof different semantic categories selective damage to the visualor the functional semantic subsystem will result in a category-like decit A review of the literature and the results of a newcase of category-specic decit will show that the domain-specic knowledge framework provides a better account ofcategory-specic decits than the sensoryfunctional dichot-omy theory

INTRODUCTION

How is conceptual knowledge organized in the brainEvidence relevant to this issue is provided by the pat-terns of semantic processing decits in brain-damagedsubjects especially those decits that seem to selectivelyaffect one or another semantic category The rst cleardemonstration of a semantic category-specic decitwas made by Warrington and Shallice (1984) They re-ported four patients recovering from herpes simplexencephalitis who were disproportionately impaired inproducing and understanding the names of living thingsThis result coupled with the observation of a brain-dam-aged subject who showed the reverse dissociationmdashthatis relative sparing of the comprehension of living rela-tive to nonliving things1 (Warrington amp McCarthy1983)mdashinvited the inference that brain damage couldresult in category-specic semantic decits2

Although the four cases described by Warrington andShallice (1984) were not all tested with the same tasksor the same materials they all showed poorer perfor-mance in producing andor comprehending the namesof living as opposed to nonliving things In some casesthe contrast in performance was quite striking JBR wasonly able to recognize or name 2 of 48 living things(animals or plants) but accurately described or named45 of 48 nonliving things similarly SBY failed to iden-tify any of the living items but correctly identied 36 of48 nonliving things For example JBR dened briefcase

copy 1998 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 101 pp 1ndash34

as ldquosmall case used by students to carry papersrdquo butresponded ldquodonrsquot knowrdquo to the word parrot similarlySBY dened towel as ldquomaterial used to dry peoplerdquo butresponded ldquobird that iesrdquo to the word wasp The othertwo cases reported by Warrington and Shallice KB andING could not be tested with the denition produc-tion tasks because of their severe language productiondecits but their performance in wordpicture matchingtasks was poorer for animals than for nonliving thingsThus all four cases showed disproportionate difcultyfor living than for nonliving things

Conrmation of the dissociation of performance forliving and nonliving things was soon obtained in manyother studies of brain-damaged subjects of various etiolo-gies including other cases of herpes simplex encephali-tis trauma cerebro-vascular accident and neurosurgery(Basso Capitani amp Laiacona 1988 Damasio GrabowskiTranel Hichwa amp Damasio 1996 De Renzi amp Lucchelli1994 Farah Hammond Mehta amp Radcliff 1989 FarahMcMullen amp Meyer 1991 Hart amp Gordon 1992 Hillis ampCaramazza 1991 Laiacona Barbarotto amp Capitani 1993Laiacona Capitani amp Barbarotto 1997 McCarthy amp War-rington 1988 Pietrini Nertempi Vaglia Revello Pinna ampFerro-Milone 1988 Powell amp Davidoff 1995 Sartori ampJob 1988 Sheridan amp Humphreys 1993 Silveri amp Gai-notti 1988 Sirigu Duhamel amp Poncet 1991) And therehave also been several reports documenting the reversepattern of dissociationsmdashthat is cases of impaired per-formance in naming andor recognizing nonliving ob-

jects in the face of spared ability with living things (Hillisamp Caramazza 1991 Sacchett amp Humphreys 1992 War-rington amp McCarthy 1983 1987) It would seem thenthat the category of living things can be damaged inde-pendently of the category of nonliving things thus invit-ing the inference that the semantic system might beorganized categorically Furthermore because most ofthe patients with selective impairment of the living cate-gory had sustained damage to (at least) the left temporallobe it might be further surmised that the latter neuralstructure is part of a neural network specically dedi-cated to representing conceptual knowledge about liv-ing objects3

Despite the seemingly categorical nature of the decitthe inference that the semantic system is organized cate-gorically has never been entertained seriously (but seeWarrington 1981) The obstacle most often cited againsta categorical interpretation of the category-specic se-mantic decits was apparent from the earliest resultsThe patterns of semantic categories affected in any onepatient did not correspond to plausible clear-cut cate-gorical distinctions such as the livingnonliving or natu-ral kindartifact dichotomies For example the earlyparadigm cases JBR and SBY were both impaired notonly in processing the animal and plant categories butalso foods Clearly there is no obvious way in which thefood category could be easily subsumed within the livingthing category (think of spaghetti rice pudding etc)Furthermore extensive testing of JBR showed that hewas also impaired in dening musical instruments pre-cious stones cloths and metalsmdashall inanimate objectsmdashbut not body parts (which according to some authorsshould be associated with living things) These violationsof the simple dichotomy of livingnonliving things ledWarrington amp Shallice (1984 see also Warrington ampMcCarthy 1983 1987) to propose the sensoryfunctionaltheory of category-specic decits They argued thatfunctional and visual (sensory) attributes are not onlydifferentially important for the identication of nonlivingand living things respectively but also for other catego-ries such as food Damage to the visual semantic subsys-tem results in disproportionate impairment of thecategories of living things and foods because the iden-tication of the members of these categories dependscrucially on their visual (sensory) features and damageto the functional semantic subsystem results in dispro-portionate impairment of nonliving things because iden-tication of the members of this category of objectsdepends crucially on their functional nonsensory attrib-utes In other words the seemingly categorical nature ofsemantic decits does not reect the categorical organi-zation of conceptual knowledge in the brain but ismerely the accidental consequence of a more basicnoncategorical organizing principle of the semantic sys-tem4

The rejection of the possibility that conceptual knowl-edge might be organized categorically in the brain may

have been premature Here we show that the evidenceusually cited in favor of reductionist accounts of cate-gory-specic decits is far from compelling Howeverbefore doing so we consider whether the reported cate-gory effects are real or just artifacts of uncontrolledstimulus variables

Are Category-Specic Decits Artifacts ofUncontrolled Stimulus Factors

Warrington and Shallice (1984) raised and dismissed thepossibility that the category-specic decits they re-ported might have arisen from frequency or familiaritydifferences between the members of the living and non-living categories In an identication experiment withword and picture stimuli their subject SBY performedfar worse with the living than the nonliving categoryeven when familiarity and frequency were taken intoconsideration through covariance analyses This precau-tion has not always been observed in other studies (oreven the other cases in Warrington and Shallicersquos paper)It is not inappropriate therefore for Funnell and Sheri-dan (1992) Gaffan and Heywood (1993) and StewartParkin and Hunkin (1992) to raise the question ofwhether putative cases of category-specic decits forliving things might not simply reect the fact that theseitems tend to be of lower frequency and familiarity andmore visually complex than nonliving things This con-cern is not unfounded because frequency familiarity andvisual complexity have powerful effects on perfor-mance

Stewart et al (1992) provide the clearest demonstra-tion of the need for caution in interpreting putativecases of category-specic decit of living things Theyreport a case HO with herpes simplex encephalitiswhose performance in naming the Snodgrass and Van-derwart (1980) pictures showed a signicant categoryeffect with poorer performance for the living than non-living category (65 versus 86) The difference be-tween categories remained even when the lists werematched for word frequency (42 versus 80 for livingand nonliving respectively) However when the twocategories were matched jointly for frequency familiarityand visual complexity the category effect disappeared(42 versus 36 for living and nonliving things respec-tively) Furthermore when the categories were redenedin terms of the extent to which sensory (animals vege-tables fruit large buildings and natural features) versusfunctional (tools and kitchen utensils) attributes are sup-posedly more important in determining the meaning ofcategory members there again was no difference be-tween categories when frequency familiarity and visualcomplexity were jointly controlled (57 versus 58respectively) These results together with those of Fun-nell and Sheridan (1992) who showed that item famili-arity can be a major determinant of naming accuracy andthe results of Gaffan and Heywood (1993) who showed

2 Journal of Cognitive Neuroscience Volume 10 Number 1

that living and nonliving things differ in visual dis-criminability and consequent ease of recognition indi-cate that putative cases of selective decit of the livingcategory may not in fact be true category-specicdecits but may instead reect category nonspecicprocessing difculties that are more severe for low-frequency low-familiarity and hard-to-discriminate visualobjects

The results reported by Funnell and Sheridan (1992)Gaffan and Heywood (1993) and Stewart et al (1992)demand that we adopt a cautious stance in interpretingsupposed cases of category-specic decits Nonethe-less there is compelling evidence that not all putativecases of category-specic decits can be explained byappeal to between-category variation in item frequencyfamiliarity and visual complexity First just as was thecase for SBY (Warrington amp Shallice 1984) other casesof disproportionate difculty in naming and recognizingliving things continue to show the effect even whenfrequency familiarity and visual complexity are taken inconsideration (eg Farah Meyer amp McMullen 1996 Gai-notti amp Silveri 1996 Hart amp Gordon 1992 Kurbat 1997Laiacona Barbarotto amp Capitani 1993 Laiacona et al1997 Sartori Miozzo amp Job 1993 Sheridan amp Hum-phreys 1993) Thus for example Sartori et al retestedtheir subject Michelangelo (Sartori amp Job 1988) withanimals and artifacts matched for frequency familiarityand visual complexity and once again found that henamed animals signicantly less accurately than artifacts(30 versus 70) Second there are a number of reportsof disproportionate decit for the category of nonlivingthings (Hillis amp Caramazza 1991 Sacchett amp Humphreys1992 Warrington amp McCarthy 1983 1987)mdashthe suppos-edly easier-to-process category

Especially informative in this context is Hillis andCaramazzarsquos (1991) report of two cases with contrastingcategory-specic decits who were tested with the samestimuli on the same tasks One subject PS who hadsustained bilateral temporal lobe and left frontal damagefrom a severe blow to the head showed a disproportion-ate decit with living things the other case JJ who hadsustained left temporal lobe and basal ganglia damagefollowing a thromboembolic stroke showed a dispropor-tionate decit for inanimate objects The results reportedfor these two cases are striking over seven administra-tions of a naming test at 4 months postinjury JJ namedanimals (n = 46 in each test) and inanimate objects(including fruits and vegetables n = 98 in each test) withan average accuracy of 81 and 12 respectively PSnamed living things (animals fruits and vegetables) andnonliving things with an average accuracy of 47 and93 respectively The two subjects were tested again 13months postinjury when their performance had im-proved substantially Their respective category-specicdecits were still clearly apparent JJ named correctlyall animals but only 68 of inanimate objects PS namedcorrectly all nonliving objects but only 64 of living

things These patientsrsquo category-specic decits were notrestricted to naming tasks but extended to comprehen-sion tasks JJ demonstrated comprehension of all animalnames but dened incorrectly or gave ambiguous re-sponses to 23 of 98 nonanimal names PS understoodcorrectly all names of artifacts but dened incorrectly orgave ambiguous denitions to 11 of 70 animal namesClearly it is not possible to explain these contrastingpatterns of category-specic decits by appealing simplyto between-category variation in item frequency famili-arity andor visual complexity Indeed the selective spar-ing of the animals category in JJ unambiguouslyindicates that conceptual knowledge can be damagedalong the boundaries of semantic categories

The conclusion to be drawn from the fact that selec-tive impairment of the living category is not alwaysreducible to an effect of frequency familiarity andorvisual similarity (eg Sartori et al 1993) and the fact thatknowledge of the living category can be selectivelyspared (eg Hillis amp Caramazza 1991) is not howeverthat all putative cases of category-specic decits are tobe taken as such Funnell and Sheridanrsquos (1992) andStewart et alrsquos (1992) admonition against the facile in-terpretation of performance differences between catego-ries of items as having a categorical basis remainsgenerally validmdashit is valid for the brain-damaged subjectsthey studied and it is likely to be valid for some of theother putative cases of category-specic decit

There are at least three implications that follow fromthe foregoing discussion These concern the frequencyof occurrence of different types of category-specicdecits the types of categories affected and the puta-tively disproportionate impairment in processing visualversus functional attributes by subjects with category-specic decit for living things The rst two points areobvious if not less important because of that Althoughthere is a clear asymmetry in the number of reportedcases of living versus nonliving category-specic decits(eg Gainotti amp Silveri 1996 Saffran amp Schwartz 1994)we cannot be sure of the magnitude of the putativeasymmetry because most of the reported studies did notmatch category items on the variables of familiarity andvisual complexity Similarly although there are many re-ports of decit or sparing of one or another highlyspecic category (eg musical instruments gemstonesgeographical places outdoor objects etc) their validitymust remain in question because the items in thesecategories were also not specically controlled for nui-sance variables that might have led to their spuriouslylow or high levels of performance And as we shall arguemore extensively below the cautionary moral to bedrawn from Stewart et alrsquos (1992) paper in particularextends beyond the issue of whether a differential pat-tern of performance across categories is to be ascribeda categorical status The implications also extend toclaims about various cases of putatively disproportionateimpairment in processing visual versus functional infor-

Caramazza and Shelton 3

mation for the category of living things because in thesecases too there may have been inadequate control ofthe relative difculty of visual and functional test items

Having argued that at least some category-specicdecits are real category effects (ie not artifacts ofuncontrolled stimulus factors) we now consider indetail two reductionist accounts of category-specicdecits

The SensoryFunctional Theory

The received reductionist account of category-specicdecits is based on the role of sensory and functionalproperties in determining the meaning of living andnonliving things (Allport 1985 Gainotti amp Silveri 1996Hart amp Gordon 1992 Shallice 1988 Silveri amp Gainotti1988 Warrington amp McCarthy 1983 1987 Warrington ampShallice 1984) There are several variants of this theorybut they all share two assumptions (1) conceptualknowledge is organized in the brain by modality (visualolfactory motorfunctional etc) and (2) sensory andfunctional properties are differentially important in iden-tifying members of the living and nonliving categoriesrespectively We refer to this class of accounts as thesensoryfunctional theory (SFT)

The most widely discussed variant of this modality-based theory of semantics is the multiple semanticstheory proposed by Warrington Shallice and McCarthy(Warrington amp McCarthy 1983 1987 Warrington amp Sal-lice 1984) which draws a fundamental distinction be-tween so-called visual and verbal semantics The othercrucial assumption of the SFT is that the visual proper-ties of concepts are much more important for distin-guishing among members of living than nonliving thingsA consequence of these assumptions is that selectivedamage to the visual semantic subsystem should resultin disproportionate impairment for the living categorymdashand hence a category-specic decit A further expecta-tion derived from this model is that damage to the visualsemantic subsystem should result in disproportionatedifculty with visual properties of the living things cate-gory5 A computationally based variant of the SFT (Farahamp McClelland 1991) has conrmed the basic predictionsderived from the original proposal by Warrington Shal-lice and McCarthy

Two types of evidence have been cited in support ofthe SFT and against a categorical account of category-specic decits (1) category-specic decits supposedlydo not fall out neatly along the boundaries on which thelivingnonliving categories divide and (2) category-specic decits are supposedly also modality-specicmdashthat is subjects with selective decits for items in theliving things category are supposedly more impaired inprocessing their visual than their functional properties(although they may also be impaired in processing thelatter) We discuss these two types of evidence in turn

What Are the Categories of Category-Specic Decits

The four cases of category-specic decit described inWarrington and Shallicersquos (1984) seminal report were allimpaired in processing not only living things but alsofoods Furthermore one of the four patients who wastested with a more extensive set of categories (JBR)was also impaired with the categories of musical instru-ments precious stones diseases cloths and metals War-rington and Shallice speculated that the co-occurrenceof decits to specic categories observed in these pa-tients was not accidental but reects instead the fact thatthe meanings of the items in the impaired categoriesdepend more heavily on the same damaged semanticsubsystem That is the co-occurrence of decits for thecategories of animals foods plants and musical instru-ments was assumed to reect the fact that the meaningsof the members of these categories are distinguishedprimarily by their visual properties whereas the mem-bers of the spared categories (eg furniture vehiclestools etc) are distinguished primarily by their functionalattributes

Although one of the more robust associations of cate-gory-specic decits is that between the categories ofanimals and foods (De Renzi amp Lucchelli 1994 Sheridanamp Humphreys 1993 Silveri amp Gainotti 1988 Warringtonamp Shallice 1984) there are a number of violations to thisempirical generalization There are patients with cate-gory-specic decits who are impaired for animals (andfruits and vegetables in some cases) but not food (Hartamp Gordon 1992 case JJ Hillis amp Caramazza 1991 Laia-cona Barbarotto amp Capitani 1993) or who are impairedin naming food items but not animals (case PS Hillis ampCaramazza 1991)6 Similarly the association of decits ofliving things and musical instruments which was ob-served in some of the early reports of category-specicdecit (Silveri amp Gainotti 1988 Warrington amp Shallice1984) has not held up Thus for example the patientreported by De Renzi amp Lucchelli (1994) who wasotherwise very similar to those reported by Silveri andGainotti and by Warrington and Shallice performed verywell with musical instruments And although there havebeen a number of reports of selective damage or sparingof the category of living things (animals fruits and vege-tables eg case PS Hillis amp Caramazza 1991 LaiaconaBarbarotto amp Capitani 1993) it too dissociates but alongtheoretically interesting lines The category of animalscan be damaged or spared independently of the categoryof fruits vegetables and plants (Hillis amp Caramazza 1991Hart amp Gordon 1992) and the category of fruits andvegetables (or plants) can be damaged selectively (Farahamp Wallace 1992 Hart Berndt amp Caramazza 1985) fromother living and nonliving categories

It is far from obvious that the SFT can make sense ofthe attested patterns of associations and dissociations ofcategory-specic decits The rst problem concerns

4 Journal of Cognitive Neuroscience Volume 10 Number 1

whether it is reasonable to assume that the observedassociations of category-specic decits reect the or-ganizing principle of modality-specic semantics Thuswhat underlying sensoryfunctional principles wouldgroup together the categories of animals foods andmusical instruments versus the categories of furnituretools and body parts The mere assertion that the mean-ings of the items in the rst set are more dependent onvisual or other sensory attributes and those of the sec-ond set are more dependent on functional attributes isnot particularly convincing Consider for example thecontrast among carrot celery apple orange avocadotomato hamburger scrambled eggs pasta beer and wineThese items are clearly visually different from one an-other but they are also functionally different One mightgo so far as to contend that what is important fordiscriminating among them is not so much their visualshape but their functions used to make juice used fordessert eaten at breakfast Italian food fast food eatenraw eaten cooked used for minestrone and so on Thesame argument can be made for musical instrumentswith respect to the importance of their functional prop-erties And certainly visual shape is as important fordistinguishing hands heads beds stools hammers andscrewdrivers as is their function Nonetheless the claimthat the relative ldquoweightingrdquo of the sensory and func-tional properties for discriminating among members ofa semantic category provides the binding factor for someof the observed associations of category-specic decitshas never been developed in enough detail to allowserious consideration of its merits7

Far more damaging to the SFT is the pattern of disso-ciations of category-specic decits Since part of themotivation for the SFT is the claim that certain semanticcategories tend to be damaged together because of theircommon dependence on a modality-specic semanticsubsystem the observation that these same categoriescan be damaged independently of each other poses aserious threat to the theory That is in the measure towhich one is committed to explaining the observedco-occurrence of impairment of for example the cate-gories of animals and of fruits and vegetables as reect-ing their shared dependence on the hypothesized visualsemantic subsystem one is thereby committed to theirnecessary co-occurrence and their dissociation wouldconstitute evidence against the hypothesized semanticsubsystem

Warrington and McCarthy (1987) were keenly awareof this danger to the SFT and tried to deal with it byhypothesizing further subdivisions within the visual se-mantic subsystem They argued that the dissociation ofdecits of the categories of animals and of fruits andvegetables may be explained by assuming that someperceptual features are more important for animals thanfor fruits and vegetables and vice versa for some otherperceptual features They speculated that shape may be

more important for the categories of owers and animalsand that color may be more important for the categoryof fruits and vegetables And presumably in order toexplain the other patterns of dissociations of category-specic decits (eg animals from owers animals frommusical instruments) further subdivisions would have tobe specied within the visual and functional semanticsubsystems However no independent evidence hasbeen provided for the claim that distinction amongmembers of different semantic categories depend differ-entially on color shape or other sensory features Norhas it been shown that impairment of particular seman-tic categories is associated with special difculties forspecic types of sensory information (eg greater dif-culty processing color in patients with selective damageto the categories of fruits and vegetables) Furthermoreit should be noted that the more subdivisions one pro-poses specically in order to accommodate dissocia-tions of particular categories the more this proposalbecomes indistinguishable from a categorical account ofcategory-specic decits

The evidence and arguments presented in this sectionhave shown that one of the pillars of the SFT does nothold Contrary to the early reports of category-specicdecits that stressed the co-occurrence of conceptuallydisparate combinations of categories (eg animals foodsand musical instruments) there are a number of well-documented cases of dissociations of these categoriesAnd as we have seen there appears to be no clearlymotivated basis for the argument that attested patternsof associations and dissociations of semantic categorydecits are readily explicable in terms of selective dam-age to modality-specic semantic subsystems These criti-cisms of the SFT undermine its supposed superiorityover categorical accounts in explaining the occurrenceof category-specic decits We turn now to the othermajor argument for the SFTmdashthe claim that patientswith selective damage to the living category are dispro-portionately impaired in processing their visual proper-ties

Is Knowledge of Visual Properties More SeverelyImpaired Than Knowledge of Functional Propertiesin Individuals with Category-Specic Decits forLiving Things

The claim that semantic category-specic decits reectselective damage to the visual or to the functional8

semantic subsystems predicts that subjects with selec-tive damage to the living or the nonliving categoriesshould show disproportionate difculty with visual orfunctional properties respectively This expectation isderived not only from Warrington Shallice andMcCarthyrsquos theory (Warrington amp McCarthy 1983 1987Warrington amp Shallice 1984) of the semantic system butalso from the computational variant proposed by Farah

Caramazza and Shelton 5

and McClelland (1991) The results of several studieshave been interpreted as having conrmed this predic-tion That is there are reports of subjects with dispropor-tionate impairment of the category of living things whoare also supposedly disproportionately impaired in proc-essing the visual attributes of living things

The rst studies that explicitly addressed the possibil-ity of a co-occurrence of category- and modality-specicsemantic decits are those of Basso et al (1988) Sartoriand Job (1988)9 and Silveri and Gainotti (1988) In allthree studies it was reported that subjects with dispro-portionate difculty with living things also had dispro-portionate difculty responding to questions about thevisual attributes of living objects For example Basso etal report that their subject (NV) correctly answered 25of 29 questions about the functional attributes of livingthings (eg Does it live in Italy or in the desert) butonly 10 of 20 questions about their sensory attributes(eg Does it have a smooth back or is it humpbacked)Similarly subject LA (Silveri amp Gainotti 1988) was onlyable to name 1 of 11 animals in response to denitionsthat stressed visual attributes (eg a black and whitestriped wild horse) but could name 8 of 14 animals inresponse to denitions that stressed functional attributes(eg the king of the jungle)

Later studies also purportedly showed an associationof category- and modality-specic semantic decits (DeRenzi amp Lucchelli 1994 Farah et al 1989 Gainotti ampSilveri 1996 Hart amp Gordon 1992) Thus for exampleFarah et al report that their subject LH was dispropor-tionately impaired in answering questions about visualattributes of living things (eg Do ducks have long earsvs Is peacock served in French restaurants) And DeRenzi and Lucchelli report that their subject Felicia wassignicantly worse at answering questions about physi-cal than ldquofunctional-encyclopedicrdquo attributes of livingthings but that she showed no such difference for non-living things

Despite the seeming convergence of results in favorof the possibility that category-specic decits are alsomodality-specic there are reasons for skepticism ininterpreting these results First there are issues concern-ing the validity of the reported results in each of thestudies cited second there is growing evidence thatcategory-specic decits are not associated with dispro-portionate difculties in processing either the visual orthe functional attributes of objects

Interpretation of some of the studies purporting toshow that patients with category-specic decits forliving things are also disproportionately impaired inprocessing these objectsrsquo visual attributes is underminedby the fact that these studies failed to control the relativedifculty of visual and functional attribute judgmentsStewart et al (1992 Exp 5) have shown that judgmentsabout the visual properties of living things are moredifcult to evaluate than judgments about functionalproperties They have also shown that the disproportion-

ate difculty for visual attributes for living things in apatient with a putative category-specic decit disap-pears when visual and functional judgments are matchedfor difculty (Exp 6) In light of these results it is notpossible to meaningfully interpret some of the earlystudies claiming to show a co-occurrence of category-and modality-specic decits where no attempt wasmade to control the relative difculty of visual and func-tional attribute judgments (eg Basso et al 1988 Sartoriamp Job 1988 Silveri amp Gainotti 198810)

A related difculty is encountered by De Renzi andLucchellirsquos (1994) study Although the authors were ableto show that their subject Felicia was more severelyimpaired in processing visual attributes of living thannonliving category items she was also impaired in proc-essing functional attributes of living things as indicatedfor example by her performance in deciding whether ananimal was native of Italy (only 73 correct) Further-more since no attempt was made to equate visual andfunctional judgments for difculty it is not possible todirectly compare relative performance for the two typesof judgments

Farah et al (1989) argued that their subject LHpresented with a category-specic decit for the livingcategory that was also modality-specic for visual prop-erties However inspection of their data (Table 1 Farahet al) shows that normal subjects were also dispropor-tionately poor in answering questions about the visualproperties of the living category Thus no meaningfulconclusion concerning category-specic decits is pos-sible from this study

Recently Gainotti and Silveri (1996) retested theirsubject LA with new materials designed to be free ofthe methodological problems encountered by their ear-lier report They again showed that LA performed dis-proportionately poorly on tasks involving the processingof visual attributes of living things For example in a taskrequiring the identication of the visual feature onwhich two objects differed they found that LA per-formed worse with animals (15 correct) than artifacts(50 correct) However the two categories were alsosignicantly different in familiarity (on a scale of 1 to 5255 and 396 for animals and artifacts respectively) Andin a color feature naming task in which LA again per-formed more poorly with living than nonliving thingsthere too the two categories differed in familiarity Thusthe interpretation of LArsquos performance regarding theputative association of category- and modality-specicdecits remains problematic at best

Finally Hart and Gordon (1992) have also argued fora modality-specic organization of the semantic systemon the basis of the performance of their subject KRwho presented with a category-specic decit restrictedto animals KR performed very poorly in naming ani-mals (18 of 61) despite being perfectly normal in namingother objects (348 of 350) The striking feature of thissubject was that she could answer correctly all ques-

6 Journal of Cognitive Neuroscience Volume 10 Number 1

tions about functional attributes of animals as well as allquestions about both visual and functional attributes ofinanimate objects but was quite poor in answering ques-tions about the visual attributes of animals Thus thiscase would seem to represent the perfect dissociation insupport of the SFT11 However there are aspects of thissubjectrsquos performance that are problematic for the SFTand there are other features of her performance that mayundermine its usefulness altogether

The fact that KR was impaired in processing thevisual properties of only animals is inconsistent with theSFT The theory predicts that damage to visual semanticswould differentially affect the living and nonliving cate-gories It does not predict that it would lead to damageto only the category of animals At the very least itpredicts impairment of other living things (eg fruits)besides animals as well as less-marked impairment of thenonliving category None of these conditions were metby the results of this study Equally problematic for theSFT is the fact that KRrsquos decit in processing visualproperties of animals was restricted to language inputsShe only performed poorly with visual attributes whenshe was required to respond to verbal inputs or torespond verbally Thus for example she performed per-fectly in distinguishing between appropriately and inap-propriately colored animals but could not perform thesame discrimination when the color alternatives weregiven verbally This result is also highly problematic forthe SFT The theory predicts equal difculties (barringadditional sensory or language decits) for visual andverbal tasks because damage to the visual semantic sub-system would presumably lead to impairments in alltasks involving the use of this system Thus KRrsquos selec-tive difculty for visual properties restricted to the ver-bal domain is uninterpretable within the SFT

Perhaps most problematic about the Hart and Gordon(1992) study is their subjectrsquos performance in a forced-choice property judgment task In this task KR wasrequired to choose between two visual or two nonphysi-cal properties of animals (eg Is an elephant orange orgray or Is an elephant a food or an animal) The prop-erties were chosen in such a way that they includedproperties that she had produced correctly and incor-rectly in a previous direct recall task (eg Whatrsquos thecolor of lemon Yellow Whatrsquos the color of an elephantOrange) In this task she virtually always (186 of 187)picked the choice corresponding to the property shehad produced in the previously administered propertynaming task whether correct or incorrect Thus forexample consistent with her response in the propertyproduction task she chose orange when given thechoice Is an elephant orange or gray She chose theincorrect strange response in 54 out of 55 trials Theunexpected systematicity of KRrsquos strange errors raisesquestions about the usefulness of this study for inform-ing theories of normal language because it appears thatshe may have come to have systematic ldquostrange beliefsrdquo

about some animals12 Nevertheless the most that canbe concluded for the SFT from the Hart and Gordonstudy is that those aspects of KRrsquos performance that arenot strange are not explicable within the theory

This review of the experimental evidence cited insupport of the claim that subjects with a category-specic decit for living things are disproportionatelyimpaired in processing the visual features of conceptshas shown it to be inadequate for the stated purpose Ineach case (with the exception of Hart and Gordon 1992but there are other problems with this study) the failureto adequately control for differential levels of difcultyin processing visual versus functional properties of con-cepts undermines the possibility of drawing clear infer-ences from the results13 Thus there is no compellingempirical evidence in favor of the claim that category-specic decits are also necessarily modality-specicdecits Furthermore there is growing evidence thatsubjects with category-specic decits for living thingsare equally impaired in processing visual and functionalattributes of objectsmdashevidence that is directly in conictwith the SFT

Laiacona Barbarotto amp Capitani (1993) and Laiaconaet al (1997) have provided the clearest evidence to datefor equal levels of impairment for visual and functionalattributes in cases of category-specic decit for livingthings In the earlier of the two studies they reportedtwo trauma cases FM and GR with disproportionateimpairment in processing living things (FM 20 vs 70correct naming of living and nonliving things respec-tively GR 13 vs 73 correct naming of living andnonliving things respectively) When these subjectswere tested in a forced-choice task with strictly matchedquestions about visual or functional properties of ob-jects (Laiacona Barbarotto Trivelli amp Capitani 1993)they performed equally poorly with the two types ofattributes Thus FM responded correctly 73 and 69of the time to questions about visual and functionalproperties of living things respectively and he re-sponded correctly 96 of the time to both visual andfunctional properties of nonliving things Similarly GRresponded correctly 55 and 58 of the time to ques-tions about visual and functional properties of livingthings respectively and he responded correctly 91 ofthe time to visual properties and 84 of the time tofunctional properties of nonliving things In a more re-cent study Laiacona et al (1997) again observed equallevels of impairment for knowledge of visual and func-tional attributes in two new cases of category-specicdecit for living things14

Two other studies (Funnell amp De Mornay Davies 1997Sheridan amp Humphreys 1993) further conrm this pat-tern of results Sheridan and Humphreys reported a sub-ject with a category-specic decit for living things whowas equally impaired with visual and functional attributejudgments (14 of 20 and 13 of 20 for visual and func-tional attributes of animals respectively) And in a new

Caramazza and Shelton 7

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

jects in the face of spared ability with living things (Hillisamp Caramazza 1991 Sacchett amp Humphreys 1992 War-rington amp McCarthy 1983 1987) It would seem thenthat the category of living things can be damaged inde-pendently of the category of nonliving things thus invit-ing the inference that the semantic system might beorganized categorically Furthermore because most ofthe patients with selective impairment of the living cate-gory had sustained damage to (at least) the left temporallobe it might be further surmised that the latter neuralstructure is part of a neural network specically dedi-cated to representing conceptual knowledge about liv-ing objects3

Despite the seemingly categorical nature of the decitthe inference that the semantic system is organized cate-gorically has never been entertained seriously (but seeWarrington 1981) The obstacle most often cited againsta categorical interpretation of the category-specic se-mantic decits was apparent from the earliest resultsThe patterns of semantic categories affected in any onepatient did not correspond to plausible clear-cut cate-gorical distinctions such as the livingnonliving or natu-ral kindartifact dichotomies For example the earlyparadigm cases JBR and SBY were both impaired notonly in processing the animal and plant categories butalso foods Clearly there is no obvious way in which thefood category could be easily subsumed within the livingthing category (think of spaghetti rice pudding etc)Furthermore extensive testing of JBR showed that hewas also impaired in dening musical instruments pre-cious stones cloths and metalsmdashall inanimate objectsmdashbut not body parts (which according to some authorsshould be associated with living things) These violationsof the simple dichotomy of livingnonliving things ledWarrington amp Shallice (1984 see also Warrington ampMcCarthy 1983 1987) to propose the sensoryfunctionaltheory of category-specic decits They argued thatfunctional and visual (sensory) attributes are not onlydifferentially important for the identication of nonlivingand living things respectively but also for other catego-ries such as food Damage to the visual semantic subsys-tem results in disproportionate impairment of thecategories of living things and foods because the iden-tication of the members of these categories dependscrucially on their visual (sensory) features and damageto the functional semantic subsystem results in dispro-portionate impairment of nonliving things because iden-tication of the members of this category of objectsdepends crucially on their functional nonsensory attrib-utes In other words the seemingly categorical nature ofsemantic decits does not reect the categorical organi-zation of conceptual knowledge in the brain but ismerely the accidental consequence of a more basicnoncategorical organizing principle of the semantic sys-tem4

The rejection of the possibility that conceptual knowl-edge might be organized categorically in the brain may

have been premature Here we show that the evidenceusually cited in favor of reductionist accounts of cate-gory-specic decits is far from compelling Howeverbefore doing so we consider whether the reported cate-gory effects are real or just artifacts of uncontrolledstimulus variables

Are Category-Specic Decits Artifacts ofUncontrolled Stimulus Factors

Warrington and Shallice (1984) raised and dismissed thepossibility that the category-specic decits they re-ported might have arisen from frequency or familiaritydifferences between the members of the living and non-living categories In an identication experiment withword and picture stimuli their subject SBY performedfar worse with the living than the nonliving categoryeven when familiarity and frequency were taken intoconsideration through covariance analyses This precau-tion has not always been observed in other studies (oreven the other cases in Warrington and Shallicersquos paper)It is not inappropriate therefore for Funnell and Sheri-dan (1992) Gaffan and Heywood (1993) and StewartParkin and Hunkin (1992) to raise the question ofwhether putative cases of category-specic decits forliving things might not simply reect the fact that theseitems tend to be of lower frequency and familiarity andmore visually complex than nonliving things This con-cern is not unfounded because frequency familiarity andvisual complexity have powerful effects on perfor-mance

Stewart et al (1992) provide the clearest demonstra-tion of the need for caution in interpreting putativecases of category-specic decit of living things Theyreport a case HO with herpes simplex encephalitiswhose performance in naming the Snodgrass and Van-derwart (1980) pictures showed a signicant categoryeffect with poorer performance for the living than non-living category (65 versus 86) The difference be-tween categories remained even when the lists werematched for word frequency (42 versus 80 for livingand nonliving respectively) However when the twocategories were matched jointly for frequency familiarityand visual complexity the category effect disappeared(42 versus 36 for living and nonliving things respec-tively) Furthermore when the categories were redenedin terms of the extent to which sensory (animals vege-tables fruit large buildings and natural features) versusfunctional (tools and kitchen utensils) attributes are sup-posedly more important in determining the meaning ofcategory members there again was no difference be-tween categories when frequency familiarity and visualcomplexity were jointly controlled (57 versus 58respectively) These results together with those of Fun-nell and Sheridan (1992) who showed that item famili-arity can be a major determinant of naming accuracy andthe results of Gaffan and Heywood (1993) who showed

2 Journal of Cognitive Neuroscience Volume 10 Number 1

that living and nonliving things differ in visual dis-criminability and consequent ease of recognition indi-cate that putative cases of selective decit of the livingcategory may not in fact be true category-specicdecits but may instead reect category nonspecicprocessing difculties that are more severe for low-frequency low-familiarity and hard-to-discriminate visualobjects

The results reported by Funnell and Sheridan (1992)Gaffan and Heywood (1993) and Stewart et al (1992)demand that we adopt a cautious stance in interpretingsupposed cases of category-specic decits Nonethe-less there is compelling evidence that not all putativecases of category-specic decits can be explained byappeal to between-category variation in item frequencyfamiliarity and visual complexity First just as was thecase for SBY (Warrington amp Shallice 1984) other casesof disproportionate difculty in naming and recognizingliving things continue to show the effect even whenfrequency familiarity and visual complexity are taken inconsideration (eg Farah Meyer amp McMullen 1996 Gai-notti amp Silveri 1996 Hart amp Gordon 1992 Kurbat 1997Laiacona Barbarotto amp Capitani 1993 Laiacona et al1997 Sartori Miozzo amp Job 1993 Sheridan amp Hum-phreys 1993) Thus for example Sartori et al retestedtheir subject Michelangelo (Sartori amp Job 1988) withanimals and artifacts matched for frequency familiarityand visual complexity and once again found that henamed animals signicantly less accurately than artifacts(30 versus 70) Second there are a number of reportsof disproportionate decit for the category of nonlivingthings (Hillis amp Caramazza 1991 Sacchett amp Humphreys1992 Warrington amp McCarthy 1983 1987)mdashthe suppos-edly easier-to-process category

Especially informative in this context is Hillis andCaramazzarsquos (1991) report of two cases with contrastingcategory-specic decits who were tested with the samestimuli on the same tasks One subject PS who hadsustained bilateral temporal lobe and left frontal damagefrom a severe blow to the head showed a disproportion-ate decit with living things the other case JJ who hadsustained left temporal lobe and basal ganglia damagefollowing a thromboembolic stroke showed a dispropor-tionate decit for inanimate objects The results reportedfor these two cases are striking over seven administra-tions of a naming test at 4 months postinjury JJ namedanimals (n = 46 in each test) and inanimate objects(including fruits and vegetables n = 98 in each test) withan average accuracy of 81 and 12 respectively PSnamed living things (animals fruits and vegetables) andnonliving things with an average accuracy of 47 and93 respectively The two subjects were tested again 13months postinjury when their performance had im-proved substantially Their respective category-specicdecits were still clearly apparent JJ named correctlyall animals but only 68 of inanimate objects PS namedcorrectly all nonliving objects but only 64 of living

things These patientsrsquo category-specic decits were notrestricted to naming tasks but extended to comprehen-sion tasks JJ demonstrated comprehension of all animalnames but dened incorrectly or gave ambiguous re-sponses to 23 of 98 nonanimal names PS understoodcorrectly all names of artifacts but dened incorrectly orgave ambiguous denitions to 11 of 70 animal namesClearly it is not possible to explain these contrastingpatterns of category-specic decits by appealing simplyto between-category variation in item frequency famili-arity andor visual complexity Indeed the selective spar-ing of the animals category in JJ unambiguouslyindicates that conceptual knowledge can be damagedalong the boundaries of semantic categories

The conclusion to be drawn from the fact that selec-tive impairment of the living category is not alwaysreducible to an effect of frequency familiarity andorvisual similarity (eg Sartori et al 1993) and the fact thatknowledge of the living category can be selectivelyspared (eg Hillis amp Caramazza 1991) is not howeverthat all putative cases of category-specic decits are tobe taken as such Funnell and Sheridanrsquos (1992) andStewart et alrsquos (1992) admonition against the facile in-terpretation of performance differences between catego-ries of items as having a categorical basis remainsgenerally validmdashit is valid for the brain-damaged subjectsthey studied and it is likely to be valid for some of theother putative cases of category-specic decit

There are at least three implications that follow fromthe foregoing discussion These concern the frequencyof occurrence of different types of category-specicdecits the types of categories affected and the puta-tively disproportionate impairment in processing visualversus functional attributes by subjects with category-specic decit for living things The rst two points areobvious if not less important because of that Althoughthere is a clear asymmetry in the number of reportedcases of living versus nonliving category-specic decits(eg Gainotti amp Silveri 1996 Saffran amp Schwartz 1994)we cannot be sure of the magnitude of the putativeasymmetry because most of the reported studies did notmatch category items on the variables of familiarity andvisual complexity Similarly although there are many re-ports of decit or sparing of one or another highlyspecic category (eg musical instruments gemstonesgeographical places outdoor objects etc) their validitymust remain in question because the items in thesecategories were also not specically controlled for nui-sance variables that might have led to their spuriouslylow or high levels of performance And as we shall arguemore extensively below the cautionary moral to bedrawn from Stewart et alrsquos (1992) paper in particularextends beyond the issue of whether a differential pat-tern of performance across categories is to be ascribeda categorical status The implications also extend toclaims about various cases of putatively disproportionateimpairment in processing visual versus functional infor-

Caramazza and Shelton 3

mation for the category of living things because in thesecases too there may have been inadequate control ofthe relative difculty of visual and functional test items

Having argued that at least some category-specicdecits are real category effects (ie not artifacts ofuncontrolled stimulus factors) we now consider indetail two reductionist accounts of category-specicdecits

The SensoryFunctional Theory

The received reductionist account of category-specicdecits is based on the role of sensory and functionalproperties in determining the meaning of living andnonliving things (Allport 1985 Gainotti amp Silveri 1996Hart amp Gordon 1992 Shallice 1988 Silveri amp Gainotti1988 Warrington amp McCarthy 1983 1987 Warrington ampShallice 1984) There are several variants of this theorybut they all share two assumptions (1) conceptualknowledge is organized in the brain by modality (visualolfactory motorfunctional etc) and (2) sensory andfunctional properties are differentially important in iden-tifying members of the living and nonliving categoriesrespectively We refer to this class of accounts as thesensoryfunctional theory (SFT)

The most widely discussed variant of this modality-based theory of semantics is the multiple semanticstheory proposed by Warrington Shallice and McCarthy(Warrington amp McCarthy 1983 1987 Warrington amp Sal-lice 1984) which draws a fundamental distinction be-tween so-called visual and verbal semantics The othercrucial assumption of the SFT is that the visual proper-ties of concepts are much more important for distin-guishing among members of living than nonliving thingsA consequence of these assumptions is that selectivedamage to the visual semantic subsystem should resultin disproportionate impairment for the living categorymdashand hence a category-specic decit A further expecta-tion derived from this model is that damage to the visualsemantic subsystem should result in disproportionatedifculty with visual properties of the living things cate-gory5 A computationally based variant of the SFT (Farahamp McClelland 1991) has conrmed the basic predictionsderived from the original proposal by Warrington Shal-lice and McCarthy

Two types of evidence have been cited in support ofthe SFT and against a categorical account of category-specic decits (1) category-specic decits supposedlydo not fall out neatly along the boundaries on which thelivingnonliving categories divide and (2) category-specic decits are supposedly also modality-specicmdashthat is subjects with selective decits for items in theliving things category are supposedly more impaired inprocessing their visual than their functional properties(although they may also be impaired in processing thelatter) We discuss these two types of evidence in turn

What Are the Categories of Category-Specic Decits

The four cases of category-specic decit described inWarrington and Shallicersquos (1984) seminal report were allimpaired in processing not only living things but alsofoods Furthermore one of the four patients who wastested with a more extensive set of categories (JBR)was also impaired with the categories of musical instru-ments precious stones diseases cloths and metals War-rington and Shallice speculated that the co-occurrenceof decits to specic categories observed in these pa-tients was not accidental but reects instead the fact thatthe meanings of the items in the impaired categoriesdepend more heavily on the same damaged semanticsubsystem That is the co-occurrence of decits for thecategories of animals foods plants and musical instru-ments was assumed to reect the fact that the meaningsof the members of these categories are distinguishedprimarily by their visual properties whereas the mem-bers of the spared categories (eg furniture vehiclestools etc) are distinguished primarily by their functionalattributes

Although one of the more robust associations of cate-gory-specic decits is that between the categories ofanimals and foods (De Renzi amp Lucchelli 1994 Sheridanamp Humphreys 1993 Silveri amp Gainotti 1988 Warringtonamp Shallice 1984) there are a number of violations to thisempirical generalization There are patients with cate-gory-specic decits who are impaired for animals (andfruits and vegetables in some cases) but not food (Hartamp Gordon 1992 case JJ Hillis amp Caramazza 1991 Laia-cona Barbarotto amp Capitani 1993) or who are impairedin naming food items but not animals (case PS Hillis ampCaramazza 1991)6 Similarly the association of decits ofliving things and musical instruments which was ob-served in some of the early reports of category-specicdecit (Silveri amp Gainotti 1988 Warrington amp Shallice1984) has not held up Thus for example the patientreported by De Renzi amp Lucchelli (1994) who wasotherwise very similar to those reported by Silveri andGainotti and by Warrington and Shallice performed verywell with musical instruments And although there havebeen a number of reports of selective damage or sparingof the category of living things (animals fruits and vege-tables eg case PS Hillis amp Caramazza 1991 LaiaconaBarbarotto amp Capitani 1993) it too dissociates but alongtheoretically interesting lines The category of animalscan be damaged or spared independently of the categoryof fruits vegetables and plants (Hillis amp Caramazza 1991Hart amp Gordon 1992) and the category of fruits andvegetables (or plants) can be damaged selectively (Farahamp Wallace 1992 Hart Berndt amp Caramazza 1985) fromother living and nonliving categories

It is far from obvious that the SFT can make sense ofthe attested patterns of associations and dissociations ofcategory-specic decits The rst problem concerns

4 Journal of Cognitive Neuroscience Volume 10 Number 1

whether it is reasonable to assume that the observedassociations of category-specic decits reect the or-ganizing principle of modality-specic semantics Thuswhat underlying sensoryfunctional principles wouldgroup together the categories of animals foods andmusical instruments versus the categories of furnituretools and body parts The mere assertion that the mean-ings of the items in the rst set are more dependent onvisual or other sensory attributes and those of the sec-ond set are more dependent on functional attributes isnot particularly convincing Consider for example thecontrast among carrot celery apple orange avocadotomato hamburger scrambled eggs pasta beer and wineThese items are clearly visually different from one an-other but they are also functionally different One mightgo so far as to contend that what is important fordiscriminating among them is not so much their visualshape but their functions used to make juice used fordessert eaten at breakfast Italian food fast food eatenraw eaten cooked used for minestrone and so on Thesame argument can be made for musical instrumentswith respect to the importance of their functional prop-erties And certainly visual shape is as important fordistinguishing hands heads beds stools hammers andscrewdrivers as is their function Nonetheless the claimthat the relative ldquoweightingrdquo of the sensory and func-tional properties for discriminating among members ofa semantic category provides the binding factor for someof the observed associations of category-specic decitshas never been developed in enough detail to allowserious consideration of its merits7

Far more damaging to the SFT is the pattern of disso-ciations of category-specic decits Since part of themotivation for the SFT is the claim that certain semanticcategories tend to be damaged together because of theircommon dependence on a modality-specic semanticsubsystem the observation that these same categoriescan be damaged independently of each other poses aserious threat to the theory That is in the measure towhich one is committed to explaining the observedco-occurrence of impairment of for example the cate-gories of animals and of fruits and vegetables as reect-ing their shared dependence on the hypothesized visualsemantic subsystem one is thereby committed to theirnecessary co-occurrence and their dissociation wouldconstitute evidence against the hypothesized semanticsubsystem

Warrington and McCarthy (1987) were keenly awareof this danger to the SFT and tried to deal with it byhypothesizing further subdivisions within the visual se-mantic subsystem They argued that the dissociation ofdecits of the categories of animals and of fruits andvegetables may be explained by assuming that someperceptual features are more important for animals thanfor fruits and vegetables and vice versa for some otherperceptual features They speculated that shape may be

more important for the categories of owers and animalsand that color may be more important for the categoryof fruits and vegetables And presumably in order toexplain the other patterns of dissociations of category-specic decits (eg animals from owers animals frommusical instruments) further subdivisions would have tobe specied within the visual and functional semanticsubsystems However no independent evidence hasbeen provided for the claim that distinction amongmembers of different semantic categories depend differ-entially on color shape or other sensory features Norhas it been shown that impairment of particular seman-tic categories is associated with special difculties forspecic types of sensory information (eg greater dif-culty processing color in patients with selective damageto the categories of fruits and vegetables) Furthermoreit should be noted that the more subdivisions one pro-poses specically in order to accommodate dissocia-tions of particular categories the more this proposalbecomes indistinguishable from a categorical account ofcategory-specic decits

The evidence and arguments presented in this sectionhave shown that one of the pillars of the SFT does nothold Contrary to the early reports of category-specicdecits that stressed the co-occurrence of conceptuallydisparate combinations of categories (eg animals foodsand musical instruments) there are a number of well-documented cases of dissociations of these categoriesAnd as we have seen there appears to be no clearlymotivated basis for the argument that attested patternsof associations and dissociations of semantic categorydecits are readily explicable in terms of selective dam-age to modality-specic semantic subsystems These criti-cisms of the SFT undermine its supposed superiorityover categorical accounts in explaining the occurrenceof category-specic decits We turn now to the othermajor argument for the SFTmdashthe claim that patientswith selective damage to the living category are dispro-portionately impaired in processing their visual proper-ties

Is Knowledge of Visual Properties More SeverelyImpaired Than Knowledge of Functional Propertiesin Individuals with Category-Specic Decits forLiving Things

The claim that semantic category-specic decits reectselective damage to the visual or to the functional8

semantic subsystems predicts that subjects with selec-tive damage to the living or the nonliving categoriesshould show disproportionate difculty with visual orfunctional properties respectively This expectation isderived not only from Warrington Shallice andMcCarthyrsquos theory (Warrington amp McCarthy 1983 1987Warrington amp Shallice 1984) of the semantic system butalso from the computational variant proposed by Farah

Caramazza and Shelton 5

and McClelland (1991) The results of several studieshave been interpreted as having conrmed this predic-tion That is there are reports of subjects with dispropor-tionate impairment of the category of living things whoare also supposedly disproportionately impaired in proc-essing the visual attributes of living things

The rst studies that explicitly addressed the possibil-ity of a co-occurrence of category- and modality-specicsemantic decits are those of Basso et al (1988) Sartoriand Job (1988)9 and Silveri and Gainotti (1988) In allthree studies it was reported that subjects with dispro-portionate difculty with living things also had dispro-portionate difculty responding to questions about thevisual attributes of living objects For example Basso etal report that their subject (NV) correctly answered 25of 29 questions about the functional attributes of livingthings (eg Does it live in Italy or in the desert) butonly 10 of 20 questions about their sensory attributes(eg Does it have a smooth back or is it humpbacked)Similarly subject LA (Silveri amp Gainotti 1988) was onlyable to name 1 of 11 animals in response to denitionsthat stressed visual attributes (eg a black and whitestriped wild horse) but could name 8 of 14 animals inresponse to denitions that stressed functional attributes(eg the king of the jungle)

Later studies also purportedly showed an associationof category- and modality-specic semantic decits (DeRenzi amp Lucchelli 1994 Farah et al 1989 Gainotti ampSilveri 1996 Hart amp Gordon 1992) Thus for exampleFarah et al report that their subject LH was dispropor-tionately impaired in answering questions about visualattributes of living things (eg Do ducks have long earsvs Is peacock served in French restaurants) And DeRenzi and Lucchelli report that their subject Felicia wassignicantly worse at answering questions about physi-cal than ldquofunctional-encyclopedicrdquo attributes of livingthings but that she showed no such difference for non-living things

Despite the seeming convergence of results in favorof the possibility that category-specic decits are alsomodality-specic there are reasons for skepticism ininterpreting these results First there are issues concern-ing the validity of the reported results in each of thestudies cited second there is growing evidence thatcategory-specic decits are not associated with dispro-portionate difculties in processing either the visual orthe functional attributes of objects

Interpretation of some of the studies purporting toshow that patients with category-specic decits forliving things are also disproportionately impaired inprocessing these objectsrsquo visual attributes is underminedby the fact that these studies failed to control the relativedifculty of visual and functional attribute judgmentsStewart et al (1992 Exp 5) have shown that judgmentsabout the visual properties of living things are moredifcult to evaluate than judgments about functionalproperties They have also shown that the disproportion-

ate difculty for visual attributes for living things in apatient with a putative category-specic decit disap-pears when visual and functional judgments are matchedfor difculty (Exp 6) In light of these results it is notpossible to meaningfully interpret some of the earlystudies claiming to show a co-occurrence of category-and modality-specic decits where no attempt wasmade to control the relative difculty of visual and func-tional attribute judgments (eg Basso et al 1988 Sartoriamp Job 1988 Silveri amp Gainotti 198810)

A related difculty is encountered by De Renzi andLucchellirsquos (1994) study Although the authors were ableto show that their subject Felicia was more severelyimpaired in processing visual attributes of living thannonliving category items she was also impaired in proc-essing functional attributes of living things as indicatedfor example by her performance in deciding whether ananimal was native of Italy (only 73 correct) Further-more since no attempt was made to equate visual andfunctional judgments for difculty it is not possible todirectly compare relative performance for the two typesof judgments

Farah et al (1989) argued that their subject LHpresented with a category-specic decit for the livingcategory that was also modality-specic for visual prop-erties However inspection of their data (Table 1 Farahet al) shows that normal subjects were also dispropor-tionately poor in answering questions about the visualproperties of the living category Thus no meaningfulconclusion concerning category-specic decits is pos-sible from this study

Recently Gainotti and Silveri (1996) retested theirsubject LA with new materials designed to be free ofthe methodological problems encountered by their ear-lier report They again showed that LA performed dis-proportionately poorly on tasks involving the processingof visual attributes of living things For example in a taskrequiring the identication of the visual feature onwhich two objects differed they found that LA per-formed worse with animals (15 correct) than artifacts(50 correct) However the two categories were alsosignicantly different in familiarity (on a scale of 1 to 5255 and 396 for animals and artifacts respectively) Andin a color feature naming task in which LA again per-formed more poorly with living than nonliving thingsthere too the two categories differed in familiarity Thusthe interpretation of LArsquos performance regarding theputative association of category- and modality-specicdecits remains problematic at best

Finally Hart and Gordon (1992) have also argued fora modality-specic organization of the semantic systemon the basis of the performance of their subject KRwho presented with a category-specic decit restrictedto animals KR performed very poorly in naming ani-mals (18 of 61) despite being perfectly normal in namingother objects (348 of 350) The striking feature of thissubject was that she could answer correctly all ques-

6 Journal of Cognitive Neuroscience Volume 10 Number 1

tions about functional attributes of animals as well as allquestions about both visual and functional attributes ofinanimate objects but was quite poor in answering ques-tions about the visual attributes of animals Thus thiscase would seem to represent the perfect dissociation insupport of the SFT11 However there are aspects of thissubjectrsquos performance that are problematic for the SFTand there are other features of her performance that mayundermine its usefulness altogether

The fact that KR was impaired in processing thevisual properties of only animals is inconsistent with theSFT The theory predicts that damage to visual semanticswould differentially affect the living and nonliving cate-gories It does not predict that it would lead to damageto only the category of animals At the very least itpredicts impairment of other living things (eg fruits)besides animals as well as less-marked impairment of thenonliving category None of these conditions were metby the results of this study Equally problematic for theSFT is the fact that KRrsquos decit in processing visualproperties of animals was restricted to language inputsShe only performed poorly with visual attributes whenshe was required to respond to verbal inputs or torespond verbally Thus for example she performed per-fectly in distinguishing between appropriately and inap-propriately colored animals but could not perform thesame discrimination when the color alternatives weregiven verbally This result is also highly problematic forthe SFT The theory predicts equal difculties (barringadditional sensory or language decits) for visual andverbal tasks because damage to the visual semantic sub-system would presumably lead to impairments in alltasks involving the use of this system Thus KRrsquos selec-tive difculty for visual properties restricted to the ver-bal domain is uninterpretable within the SFT

Perhaps most problematic about the Hart and Gordon(1992) study is their subjectrsquos performance in a forced-choice property judgment task In this task KR wasrequired to choose between two visual or two nonphysi-cal properties of animals (eg Is an elephant orange orgray or Is an elephant a food or an animal) The prop-erties were chosen in such a way that they includedproperties that she had produced correctly and incor-rectly in a previous direct recall task (eg Whatrsquos thecolor of lemon Yellow Whatrsquos the color of an elephantOrange) In this task she virtually always (186 of 187)picked the choice corresponding to the property shehad produced in the previously administered propertynaming task whether correct or incorrect Thus forexample consistent with her response in the propertyproduction task she chose orange when given thechoice Is an elephant orange or gray She chose theincorrect strange response in 54 out of 55 trials Theunexpected systematicity of KRrsquos strange errors raisesquestions about the usefulness of this study for inform-ing theories of normal language because it appears thatshe may have come to have systematic ldquostrange beliefsrdquo

about some animals12 Nevertheless the most that canbe concluded for the SFT from the Hart and Gordonstudy is that those aspects of KRrsquos performance that arenot strange are not explicable within the theory

This review of the experimental evidence cited insupport of the claim that subjects with a category-specic decit for living things are disproportionatelyimpaired in processing the visual features of conceptshas shown it to be inadequate for the stated purpose Ineach case (with the exception of Hart and Gordon 1992but there are other problems with this study) the failureto adequately control for differential levels of difcultyin processing visual versus functional properties of con-cepts undermines the possibility of drawing clear infer-ences from the results13 Thus there is no compellingempirical evidence in favor of the claim that category-specic decits are also necessarily modality-specicdecits Furthermore there is growing evidence thatsubjects with category-specic decits for living thingsare equally impaired in processing visual and functionalattributes of objectsmdashevidence that is directly in conictwith the SFT

Laiacona Barbarotto amp Capitani (1993) and Laiaconaet al (1997) have provided the clearest evidence to datefor equal levels of impairment for visual and functionalattributes in cases of category-specic decit for livingthings In the earlier of the two studies they reportedtwo trauma cases FM and GR with disproportionateimpairment in processing living things (FM 20 vs 70correct naming of living and nonliving things respec-tively GR 13 vs 73 correct naming of living andnonliving things respectively) When these subjectswere tested in a forced-choice task with strictly matchedquestions about visual or functional properties of ob-jects (Laiacona Barbarotto Trivelli amp Capitani 1993)they performed equally poorly with the two types ofattributes Thus FM responded correctly 73 and 69of the time to questions about visual and functionalproperties of living things respectively and he re-sponded correctly 96 of the time to both visual andfunctional properties of nonliving things Similarly GRresponded correctly 55 and 58 of the time to ques-tions about visual and functional properties of livingthings respectively and he responded correctly 91 ofthe time to visual properties and 84 of the time tofunctional properties of nonliving things In a more re-cent study Laiacona et al (1997) again observed equallevels of impairment for knowledge of visual and func-tional attributes in two new cases of category-specicdecit for living things14

Two other studies (Funnell amp De Mornay Davies 1997Sheridan amp Humphreys 1993) further conrm this pat-tern of results Sheridan and Humphreys reported a sub-ject with a category-specic decit for living things whowas equally impaired with visual and functional attributejudgments (14 of 20 and 13 of 20 for visual and func-tional attributes of animals respectively) And in a new

Caramazza and Shelton 7

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

that living and nonliving things differ in visual dis-criminability and consequent ease of recognition indi-cate that putative cases of selective decit of the livingcategory may not in fact be true category-specicdecits but may instead reect category nonspecicprocessing difculties that are more severe for low-frequency low-familiarity and hard-to-discriminate visualobjects

The results reported by Funnell and Sheridan (1992)Gaffan and Heywood (1993) and Stewart et al (1992)demand that we adopt a cautious stance in interpretingsupposed cases of category-specic decits Nonethe-less there is compelling evidence that not all putativecases of category-specic decits can be explained byappeal to between-category variation in item frequencyfamiliarity and visual complexity First just as was thecase for SBY (Warrington amp Shallice 1984) other casesof disproportionate difculty in naming and recognizingliving things continue to show the effect even whenfrequency familiarity and visual complexity are taken inconsideration (eg Farah Meyer amp McMullen 1996 Gai-notti amp Silveri 1996 Hart amp Gordon 1992 Kurbat 1997Laiacona Barbarotto amp Capitani 1993 Laiacona et al1997 Sartori Miozzo amp Job 1993 Sheridan amp Hum-phreys 1993) Thus for example Sartori et al retestedtheir subject Michelangelo (Sartori amp Job 1988) withanimals and artifacts matched for frequency familiarityand visual complexity and once again found that henamed animals signicantly less accurately than artifacts(30 versus 70) Second there are a number of reportsof disproportionate decit for the category of nonlivingthings (Hillis amp Caramazza 1991 Sacchett amp Humphreys1992 Warrington amp McCarthy 1983 1987)mdashthe suppos-edly easier-to-process category

Especially informative in this context is Hillis andCaramazzarsquos (1991) report of two cases with contrastingcategory-specic decits who were tested with the samestimuli on the same tasks One subject PS who hadsustained bilateral temporal lobe and left frontal damagefrom a severe blow to the head showed a disproportion-ate decit with living things the other case JJ who hadsustained left temporal lobe and basal ganglia damagefollowing a thromboembolic stroke showed a dispropor-tionate decit for inanimate objects The results reportedfor these two cases are striking over seven administra-tions of a naming test at 4 months postinjury JJ namedanimals (n = 46 in each test) and inanimate objects(including fruits and vegetables n = 98 in each test) withan average accuracy of 81 and 12 respectively PSnamed living things (animals fruits and vegetables) andnonliving things with an average accuracy of 47 and93 respectively The two subjects were tested again 13months postinjury when their performance had im-proved substantially Their respective category-specicdecits were still clearly apparent JJ named correctlyall animals but only 68 of inanimate objects PS namedcorrectly all nonliving objects but only 64 of living

things These patientsrsquo category-specic decits were notrestricted to naming tasks but extended to comprehen-sion tasks JJ demonstrated comprehension of all animalnames but dened incorrectly or gave ambiguous re-sponses to 23 of 98 nonanimal names PS understoodcorrectly all names of artifacts but dened incorrectly orgave ambiguous denitions to 11 of 70 animal namesClearly it is not possible to explain these contrastingpatterns of category-specic decits by appealing simplyto between-category variation in item frequency famili-arity andor visual complexity Indeed the selective spar-ing of the animals category in JJ unambiguouslyindicates that conceptual knowledge can be damagedalong the boundaries of semantic categories

The conclusion to be drawn from the fact that selec-tive impairment of the living category is not alwaysreducible to an effect of frequency familiarity andorvisual similarity (eg Sartori et al 1993) and the fact thatknowledge of the living category can be selectivelyspared (eg Hillis amp Caramazza 1991) is not howeverthat all putative cases of category-specic decits are tobe taken as such Funnell and Sheridanrsquos (1992) andStewart et alrsquos (1992) admonition against the facile in-terpretation of performance differences between catego-ries of items as having a categorical basis remainsgenerally validmdashit is valid for the brain-damaged subjectsthey studied and it is likely to be valid for some of theother putative cases of category-specic decit

There are at least three implications that follow fromthe foregoing discussion These concern the frequencyof occurrence of different types of category-specicdecits the types of categories affected and the puta-tively disproportionate impairment in processing visualversus functional attributes by subjects with category-specic decit for living things The rst two points areobvious if not less important because of that Althoughthere is a clear asymmetry in the number of reportedcases of living versus nonliving category-specic decits(eg Gainotti amp Silveri 1996 Saffran amp Schwartz 1994)we cannot be sure of the magnitude of the putativeasymmetry because most of the reported studies did notmatch category items on the variables of familiarity andvisual complexity Similarly although there are many re-ports of decit or sparing of one or another highlyspecic category (eg musical instruments gemstonesgeographical places outdoor objects etc) their validitymust remain in question because the items in thesecategories were also not specically controlled for nui-sance variables that might have led to their spuriouslylow or high levels of performance And as we shall arguemore extensively below the cautionary moral to bedrawn from Stewart et alrsquos (1992) paper in particularextends beyond the issue of whether a differential pat-tern of performance across categories is to be ascribeda categorical status The implications also extend toclaims about various cases of putatively disproportionateimpairment in processing visual versus functional infor-

Caramazza and Shelton 3

mation for the category of living things because in thesecases too there may have been inadequate control ofthe relative difculty of visual and functional test items

Having argued that at least some category-specicdecits are real category effects (ie not artifacts ofuncontrolled stimulus factors) we now consider indetail two reductionist accounts of category-specicdecits

The SensoryFunctional Theory

The received reductionist account of category-specicdecits is based on the role of sensory and functionalproperties in determining the meaning of living andnonliving things (Allport 1985 Gainotti amp Silveri 1996Hart amp Gordon 1992 Shallice 1988 Silveri amp Gainotti1988 Warrington amp McCarthy 1983 1987 Warrington ampShallice 1984) There are several variants of this theorybut they all share two assumptions (1) conceptualknowledge is organized in the brain by modality (visualolfactory motorfunctional etc) and (2) sensory andfunctional properties are differentially important in iden-tifying members of the living and nonliving categoriesrespectively We refer to this class of accounts as thesensoryfunctional theory (SFT)

The most widely discussed variant of this modality-based theory of semantics is the multiple semanticstheory proposed by Warrington Shallice and McCarthy(Warrington amp McCarthy 1983 1987 Warrington amp Sal-lice 1984) which draws a fundamental distinction be-tween so-called visual and verbal semantics The othercrucial assumption of the SFT is that the visual proper-ties of concepts are much more important for distin-guishing among members of living than nonliving thingsA consequence of these assumptions is that selectivedamage to the visual semantic subsystem should resultin disproportionate impairment for the living categorymdashand hence a category-specic decit A further expecta-tion derived from this model is that damage to the visualsemantic subsystem should result in disproportionatedifculty with visual properties of the living things cate-gory5 A computationally based variant of the SFT (Farahamp McClelland 1991) has conrmed the basic predictionsderived from the original proposal by Warrington Shal-lice and McCarthy

Two types of evidence have been cited in support ofthe SFT and against a categorical account of category-specic decits (1) category-specic decits supposedlydo not fall out neatly along the boundaries on which thelivingnonliving categories divide and (2) category-specic decits are supposedly also modality-specicmdashthat is subjects with selective decits for items in theliving things category are supposedly more impaired inprocessing their visual than their functional properties(although they may also be impaired in processing thelatter) We discuss these two types of evidence in turn

What Are the Categories of Category-Specic Decits

The four cases of category-specic decit described inWarrington and Shallicersquos (1984) seminal report were allimpaired in processing not only living things but alsofoods Furthermore one of the four patients who wastested with a more extensive set of categories (JBR)was also impaired with the categories of musical instru-ments precious stones diseases cloths and metals War-rington and Shallice speculated that the co-occurrenceof decits to specic categories observed in these pa-tients was not accidental but reects instead the fact thatthe meanings of the items in the impaired categoriesdepend more heavily on the same damaged semanticsubsystem That is the co-occurrence of decits for thecategories of animals foods plants and musical instru-ments was assumed to reect the fact that the meaningsof the members of these categories are distinguishedprimarily by their visual properties whereas the mem-bers of the spared categories (eg furniture vehiclestools etc) are distinguished primarily by their functionalattributes

Although one of the more robust associations of cate-gory-specic decits is that between the categories ofanimals and foods (De Renzi amp Lucchelli 1994 Sheridanamp Humphreys 1993 Silveri amp Gainotti 1988 Warringtonamp Shallice 1984) there are a number of violations to thisempirical generalization There are patients with cate-gory-specic decits who are impaired for animals (andfruits and vegetables in some cases) but not food (Hartamp Gordon 1992 case JJ Hillis amp Caramazza 1991 Laia-cona Barbarotto amp Capitani 1993) or who are impairedin naming food items but not animals (case PS Hillis ampCaramazza 1991)6 Similarly the association of decits ofliving things and musical instruments which was ob-served in some of the early reports of category-specicdecit (Silveri amp Gainotti 1988 Warrington amp Shallice1984) has not held up Thus for example the patientreported by De Renzi amp Lucchelli (1994) who wasotherwise very similar to those reported by Silveri andGainotti and by Warrington and Shallice performed verywell with musical instruments And although there havebeen a number of reports of selective damage or sparingof the category of living things (animals fruits and vege-tables eg case PS Hillis amp Caramazza 1991 LaiaconaBarbarotto amp Capitani 1993) it too dissociates but alongtheoretically interesting lines The category of animalscan be damaged or spared independently of the categoryof fruits vegetables and plants (Hillis amp Caramazza 1991Hart amp Gordon 1992) and the category of fruits andvegetables (or plants) can be damaged selectively (Farahamp Wallace 1992 Hart Berndt amp Caramazza 1985) fromother living and nonliving categories

It is far from obvious that the SFT can make sense ofthe attested patterns of associations and dissociations ofcategory-specic decits The rst problem concerns

4 Journal of Cognitive Neuroscience Volume 10 Number 1

whether it is reasonable to assume that the observedassociations of category-specic decits reect the or-ganizing principle of modality-specic semantics Thuswhat underlying sensoryfunctional principles wouldgroup together the categories of animals foods andmusical instruments versus the categories of furnituretools and body parts The mere assertion that the mean-ings of the items in the rst set are more dependent onvisual or other sensory attributes and those of the sec-ond set are more dependent on functional attributes isnot particularly convincing Consider for example thecontrast among carrot celery apple orange avocadotomato hamburger scrambled eggs pasta beer and wineThese items are clearly visually different from one an-other but they are also functionally different One mightgo so far as to contend that what is important fordiscriminating among them is not so much their visualshape but their functions used to make juice used fordessert eaten at breakfast Italian food fast food eatenraw eaten cooked used for minestrone and so on Thesame argument can be made for musical instrumentswith respect to the importance of their functional prop-erties And certainly visual shape is as important fordistinguishing hands heads beds stools hammers andscrewdrivers as is their function Nonetheless the claimthat the relative ldquoweightingrdquo of the sensory and func-tional properties for discriminating among members ofa semantic category provides the binding factor for someof the observed associations of category-specic decitshas never been developed in enough detail to allowserious consideration of its merits7

Far more damaging to the SFT is the pattern of disso-ciations of category-specic decits Since part of themotivation for the SFT is the claim that certain semanticcategories tend to be damaged together because of theircommon dependence on a modality-specic semanticsubsystem the observation that these same categoriescan be damaged independently of each other poses aserious threat to the theory That is in the measure towhich one is committed to explaining the observedco-occurrence of impairment of for example the cate-gories of animals and of fruits and vegetables as reect-ing their shared dependence on the hypothesized visualsemantic subsystem one is thereby committed to theirnecessary co-occurrence and their dissociation wouldconstitute evidence against the hypothesized semanticsubsystem

Warrington and McCarthy (1987) were keenly awareof this danger to the SFT and tried to deal with it byhypothesizing further subdivisions within the visual se-mantic subsystem They argued that the dissociation ofdecits of the categories of animals and of fruits andvegetables may be explained by assuming that someperceptual features are more important for animals thanfor fruits and vegetables and vice versa for some otherperceptual features They speculated that shape may be

more important for the categories of owers and animalsand that color may be more important for the categoryof fruits and vegetables And presumably in order toexplain the other patterns of dissociations of category-specic decits (eg animals from owers animals frommusical instruments) further subdivisions would have tobe specied within the visual and functional semanticsubsystems However no independent evidence hasbeen provided for the claim that distinction amongmembers of different semantic categories depend differ-entially on color shape or other sensory features Norhas it been shown that impairment of particular seman-tic categories is associated with special difculties forspecic types of sensory information (eg greater dif-culty processing color in patients with selective damageto the categories of fruits and vegetables) Furthermoreit should be noted that the more subdivisions one pro-poses specically in order to accommodate dissocia-tions of particular categories the more this proposalbecomes indistinguishable from a categorical account ofcategory-specic decits

The evidence and arguments presented in this sectionhave shown that one of the pillars of the SFT does nothold Contrary to the early reports of category-specicdecits that stressed the co-occurrence of conceptuallydisparate combinations of categories (eg animals foodsand musical instruments) there are a number of well-documented cases of dissociations of these categoriesAnd as we have seen there appears to be no clearlymotivated basis for the argument that attested patternsof associations and dissociations of semantic categorydecits are readily explicable in terms of selective dam-age to modality-specic semantic subsystems These criti-cisms of the SFT undermine its supposed superiorityover categorical accounts in explaining the occurrenceof category-specic decits We turn now to the othermajor argument for the SFTmdashthe claim that patientswith selective damage to the living category are dispro-portionately impaired in processing their visual proper-ties

Is Knowledge of Visual Properties More SeverelyImpaired Than Knowledge of Functional Propertiesin Individuals with Category-Specic Decits forLiving Things

The claim that semantic category-specic decits reectselective damage to the visual or to the functional8

semantic subsystems predicts that subjects with selec-tive damage to the living or the nonliving categoriesshould show disproportionate difculty with visual orfunctional properties respectively This expectation isderived not only from Warrington Shallice andMcCarthyrsquos theory (Warrington amp McCarthy 1983 1987Warrington amp Shallice 1984) of the semantic system butalso from the computational variant proposed by Farah

Caramazza and Shelton 5

and McClelland (1991) The results of several studieshave been interpreted as having conrmed this predic-tion That is there are reports of subjects with dispropor-tionate impairment of the category of living things whoare also supposedly disproportionately impaired in proc-essing the visual attributes of living things

The rst studies that explicitly addressed the possibil-ity of a co-occurrence of category- and modality-specicsemantic decits are those of Basso et al (1988) Sartoriand Job (1988)9 and Silveri and Gainotti (1988) In allthree studies it was reported that subjects with dispro-portionate difculty with living things also had dispro-portionate difculty responding to questions about thevisual attributes of living objects For example Basso etal report that their subject (NV) correctly answered 25of 29 questions about the functional attributes of livingthings (eg Does it live in Italy or in the desert) butonly 10 of 20 questions about their sensory attributes(eg Does it have a smooth back or is it humpbacked)Similarly subject LA (Silveri amp Gainotti 1988) was onlyable to name 1 of 11 animals in response to denitionsthat stressed visual attributes (eg a black and whitestriped wild horse) but could name 8 of 14 animals inresponse to denitions that stressed functional attributes(eg the king of the jungle)

Later studies also purportedly showed an associationof category- and modality-specic semantic decits (DeRenzi amp Lucchelli 1994 Farah et al 1989 Gainotti ampSilveri 1996 Hart amp Gordon 1992) Thus for exampleFarah et al report that their subject LH was dispropor-tionately impaired in answering questions about visualattributes of living things (eg Do ducks have long earsvs Is peacock served in French restaurants) And DeRenzi and Lucchelli report that their subject Felicia wassignicantly worse at answering questions about physi-cal than ldquofunctional-encyclopedicrdquo attributes of livingthings but that she showed no such difference for non-living things

Despite the seeming convergence of results in favorof the possibility that category-specic decits are alsomodality-specic there are reasons for skepticism ininterpreting these results First there are issues concern-ing the validity of the reported results in each of thestudies cited second there is growing evidence thatcategory-specic decits are not associated with dispro-portionate difculties in processing either the visual orthe functional attributes of objects

Interpretation of some of the studies purporting toshow that patients with category-specic decits forliving things are also disproportionately impaired inprocessing these objectsrsquo visual attributes is underminedby the fact that these studies failed to control the relativedifculty of visual and functional attribute judgmentsStewart et al (1992 Exp 5) have shown that judgmentsabout the visual properties of living things are moredifcult to evaluate than judgments about functionalproperties They have also shown that the disproportion-

ate difculty for visual attributes for living things in apatient with a putative category-specic decit disap-pears when visual and functional judgments are matchedfor difculty (Exp 6) In light of these results it is notpossible to meaningfully interpret some of the earlystudies claiming to show a co-occurrence of category-and modality-specic decits where no attempt wasmade to control the relative difculty of visual and func-tional attribute judgments (eg Basso et al 1988 Sartoriamp Job 1988 Silveri amp Gainotti 198810)

A related difculty is encountered by De Renzi andLucchellirsquos (1994) study Although the authors were ableto show that their subject Felicia was more severelyimpaired in processing visual attributes of living thannonliving category items she was also impaired in proc-essing functional attributes of living things as indicatedfor example by her performance in deciding whether ananimal was native of Italy (only 73 correct) Further-more since no attempt was made to equate visual andfunctional judgments for difculty it is not possible todirectly compare relative performance for the two typesof judgments

Farah et al (1989) argued that their subject LHpresented with a category-specic decit for the livingcategory that was also modality-specic for visual prop-erties However inspection of their data (Table 1 Farahet al) shows that normal subjects were also dispropor-tionately poor in answering questions about the visualproperties of the living category Thus no meaningfulconclusion concerning category-specic decits is pos-sible from this study

Recently Gainotti and Silveri (1996) retested theirsubject LA with new materials designed to be free ofthe methodological problems encountered by their ear-lier report They again showed that LA performed dis-proportionately poorly on tasks involving the processingof visual attributes of living things For example in a taskrequiring the identication of the visual feature onwhich two objects differed they found that LA per-formed worse with animals (15 correct) than artifacts(50 correct) However the two categories were alsosignicantly different in familiarity (on a scale of 1 to 5255 and 396 for animals and artifacts respectively) Andin a color feature naming task in which LA again per-formed more poorly with living than nonliving thingsthere too the two categories differed in familiarity Thusthe interpretation of LArsquos performance regarding theputative association of category- and modality-specicdecits remains problematic at best

Finally Hart and Gordon (1992) have also argued fora modality-specic organization of the semantic systemon the basis of the performance of their subject KRwho presented with a category-specic decit restrictedto animals KR performed very poorly in naming ani-mals (18 of 61) despite being perfectly normal in namingother objects (348 of 350) The striking feature of thissubject was that she could answer correctly all ques-

6 Journal of Cognitive Neuroscience Volume 10 Number 1

tions about functional attributes of animals as well as allquestions about both visual and functional attributes ofinanimate objects but was quite poor in answering ques-tions about the visual attributes of animals Thus thiscase would seem to represent the perfect dissociation insupport of the SFT11 However there are aspects of thissubjectrsquos performance that are problematic for the SFTand there are other features of her performance that mayundermine its usefulness altogether

The fact that KR was impaired in processing thevisual properties of only animals is inconsistent with theSFT The theory predicts that damage to visual semanticswould differentially affect the living and nonliving cate-gories It does not predict that it would lead to damageto only the category of animals At the very least itpredicts impairment of other living things (eg fruits)besides animals as well as less-marked impairment of thenonliving category None of these conditions were metby the results of this study Equally problematic for theSFT is the fact that KRrsquos decit in processing visualproperties of animals was restricted to language inputsShe only performed poorly with visual attributes whenshe was required to respond to verbal inputs or torespond verbally Thus for example she performed per-fectly in distinguishing between appropriately and inap-propriately colored animals but could not perform thesame discrimination when the color alternatives weregiven verbally This result is also highly problematic forthe SFT The theory predicts equal difculties (barringadditional sensory or language decits) for visual andverbal tasks because damage to the visual semantic sub-system would presumably lead to impairments in alltasks involving the use of this system Thus KRrsquos selec-tive difculty for visual properties restricted to the ver-bal domain is uninterpretable within the SFT

Perhaps most problematic about the Hart and Gordon(1992) study is their subjectrsquos performance in a forced-choice property judgment task In this task KR wasrequired to choose between two visual or two nonphysi-cal properties of animals (eg Is an elephant orange orgray or Is an elephant a food or an animal) The prop-erties were chosen in such a way that they includedproperties that she had produced correctly and incor-rectly in a previous direct recall task (eg Whatrsquos thecolor of lemon Yellow Whatrsquos the color of an elephantOrange) In this task she virtually always (186 of 187)picked the choice corresponding to the property shehad produced in the previously administered propertynaming task whether correct or incorrect Thus forexample consistent with her response in the propertyproduction task she chose orange when given thechoice Is an elephant orange or gray She chose theincorrect strange response in 54 out of 55 trials Theunexpected systematicity of KRrsquos strange errors raisesquestions about the usefulness of this study for inform-ing theories of normal language because it appears thatshe may have come to have systematic ldquostrange beliefsrdquo

about some animals12 Nevertheless the most that canbe concluded for the SFT from the Hart and Gordonstudy is that those aspects of KRrsquos performance that arenot strange are not explicable within the theory

This review of the experimental evidence cited insupport of the claim that subjects with a category-specic decit for living things are disproportionatelyimpaired in processing the visual features of conceptshas shown it to be inadequate for the stated purpose Ineach case (with the exception of Hart and Gordon 1992but there are other problems with this study) the failureto adequately control for differential levels of difcultyin processing visual versus functional properties of con-cepts undermines the possibility of drawing clear infer-ences from the results13 Thus there is no compellingempirical evidence in favor of the claim that category-specic decits are also necessarily modality-specicdecits Furthermore there is growing evidence thatsubjects with category-specic decits for living thingsare equally impaired in processing visual and functionalattributes of objectsmdashevidence that is directly in conictwith the SFT

Laiacona Barbarotto amp Capitani (1993) and Laiaconaet al (1997) have provided the clearest evidence to datefor equal levels of impairment for visual and functionalattributes in cases of category-specic decit for livingthings In the earlier of the two studies they reportedtwo trauma cases FM and GR with disproportionateimpairment in processing living things (FM 20 vs 70correct naming of living and nonliving things respec-tively GR 13 vs 73 correct naming of living andnonliving things respectively) When these subjectswere tested in a forced-choice task with strictly matchedquestions about visual or functional properties of ob-jects (Laiacona Barbarotto Trivelli amp Capitani 1993)they performed equally poorly with the two types ofattributes Thus FM responded correctly 73 and 69of the time to questions about visual and functionalproperties of living things respectively and he re-sponded correctly 96 of the time to both visual andfunctional properties of nonliving things Similarly GRresponded correctly 55 and 58 of the time to ques-tions about visual and functional properties of livingthings respectively and he responded correctly 91 ofthe time to visual properties and 84 of the time tofunctional properties of nonliving things In a more re-cent study Laiacona et al (1997) again observed equallevels of impairment for knowledge of visual and func-tional attributes in two new cases of category-specicdecit for living things14

Two other studies (Funnell amp De Mornay Davies 1997Sheridan amp Humphreys 1993) further conrm this pat-tern of results Sheridan and Humphreys reported a sub-ject with a category-specic decit for living things whowas equally impaired with visual and functional attributejudgments (14 of 20 and 13 of 20 for visual and func-tional attributes of animals respectively) And in a new

Caramazza and Shelton 7

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

mation for the category of living things because in thesecases too there may have been inadequate control ofthe relative difculty of visual and functional test items

Having argued that at least some category-specicdecits are real category effects (ie not artifacts ofuncontrolled stimulus factors) we now consider indetail two reductionist accounts of category-specicdecits

The SensoryFunctional Theory

The received reductionist account of category-specicdecits is based on the role of sensory and functionalproperties in determining the meaning of living andnonliving things (Allport 1985 Gainotti amp Silveri 1996Hart amp Gordon 1992 Shallice 1988 Silveri amp Gainotti1988 Warrington amp McCarthy 1983 1987 Warrington ampShallice 1984) There are several variants of this theorybut they all share two assumptions (1) conceptualknowledge is organized in the brain by modality (visualolfactory motorfunctional etc) and (2) sensory andfunctional properties are differentially important in iden-tifying members of the living and nonliving categoriesrespectively We refer to this class of accounts as thesensoryfunctional theory (SFT)

The most widely discussed variant of this modality-based theory of semantics is the multiple semanticstheory proposed by Warrington Shallice and McCarthy(Warrington amp McCarthy 1983 1987 Warrington amp Sal-lice 1984) which draws a fundamental distinction be-tween so-called visual and verbal semantics The othercrucial assumption of the SFT is that the visual proper-ties of concepts are much more important for distin-guishing among members of living than nonliving thingsA consequence of these assumptions is that selectivedamage to the visual semantic subsystem should resultin disproportionate impairment for the living categorymdashand hence a category-specic decit A further expecta-tion derived from this model is that damage to the visualsemantic subsystem should result in disproportionatedifculty with visual properties of the living things cate-gory5 A computationally based variant of the SFT (Farahamp McClelland 1991) has conrmed the basic predictionsderived from the original proposal by Warrington Shal-lice and McCarthy

Two types of evidence have been cited in support ofthe SFT and against a categorical account of category-specic decits (1) category-specic decits supposedlydo not fall out neatly along the boundaries on which thelivingnonliving categories divide and (2) category-specic decits are supposedly also modality-specicmdashthat is subjects with selective decits for items in theliving things category are supposedly more impaired inprocessing their visual than their functional properties(although they may also be impaired in processing thelatter) We discuss these two types of evidence in turn

What Are the Categories of Category-Specic Decits

The four cases of category-specic decit described inWarrington and Shallicersquos (1984) seminal report were allimpaired in processing not only living things but alsofoods Furthermore one of the four patients who wastested with a more extensive set of categories (JBR)was also impaired with the categories of musical instru-ments precious stones diseases cloths and metals War-rington and Shallice speculated that the co-occurrenceof decits to specic categories observed in these pa-tients was not accidental but reects instead the fact thatthe meanings of the items in the impaired categoriesdepend more heavily on the same damaged semanticsubsystem That is the co-occurrence of decits for thecategories of animals foods plants and musical instru-ments was assumed to reect the fact that the meaningsof the members of these categories are distinguishedprimarily by their visual properties whereas the mem-bers of the spared categories (eg furniture vehiclestools etc) are distinguished primarily by their functionalattributes

Although one of the more robust associations of cate-gory-specic decits is that between the categories ofanimals and foods (De Renzi amp Lucchelli 1994 Sheridanamp Humphreys 1993 Silveri amp Gainotti 1988 Warringtonamp Shallice 1984) there are a number of violations to thisempirical generalization There are patients with cate-gory-specic decits who are impaired for animals (andfruits and vegetables in some cases) but not food (Hartamp Gordon 1992 case JJ Hillis amp Caramazza 1991 Laia-cona Barbarotto amp Capitani 1993) or who are impairedin naming food items but not animals (case PS Hillis ampCaramazza 1991)6 Similarly the association of decits ofliving things and musical instruments which was ob-served in some of the early reports of category-specicdecit (Silveri amp Gainotti 1988 Warrington amp Shallice1984) has not held up Thus for example the patientreported by De Renzi amp Lucchelli (1994) who wasotherwise very similar to those reported by Silveri andGainotti and by Warrington and Shallice performed verywell with musical instruments And although there havebeen a number of reports of selective damage or sparingof the category of living things (animals fruits and vege-tables eg case PS Hillis amp Caramazza 1991 LaiaconaBarbarotto amp Capitani 1993) it too dissociates but alongtheoretically interesting lines The category of animalscan be damaged or spared independently of the categoryof fruits vegetables and plants (Hillis amp Caramazza 1991Hart amp Gordon 1992) and the category of fruits andvegetables (or plants) can be damaged selectively (Farahamp Wallace 1992 Hart Berndt amp Caramazza 1985) fromother living and nonliving categories

It is far from obvious that the SFT can make sense ofthe attested patterns of associations and dissociations ofcategory-specic decits The rst problem concerns

4 Journal of Cognitive Neuroscience Volume 10 Number 1

whether it is reasonable to assume that the observedassociations of category-specic decits reect the or-ganizing principle of modality-specic semantics Thuswhat underlying sensoryfunctional principles wouldgroup together the categories of animals foods andmusical instruments versus the categories of furnituretools and body parts The mere assertion that the mean-ings of the items in the rst set are more dependent onvisual or other sensory attributes and those of the sec-ond set are more dependent on functional attributes isnot particularly convincing Consider for example thecontrast among carrot celery apple orange avocadotomato hamburger scrambled eggs pasta beer and wineThese items are clearly visually different from one an-other but they are also functionally different One mightgo so far as to contend that what is important fordiscriminating among them is not so much their visualshape but their functions used to make juice used fordessert eaten at breakfast Italian food fast food eatenraw eaten cooked used for minestrone and so on Thesame argument can be made for musical instrumentswith respect to the importance of their functional prop-erties And certainly visual shape is as important fordistinguishing hands heads beds stools hammers andscrewdrivers as is their function Nonetheless the claimthat the relative ldquoweightingrdquo of the sensory and func-tional properties for discriminating among members ofa semantic category provides the binding factor for someof the observed associations of category-specic decitshas never been developed in enough detail to allowserious consideration of its merits7

Far more damaging to the SFT is the pattern of disso-ciations of category-specic decits Since part of themotivation for the SFT is the claim that certain semanticcategories tend to be damaged together because of theircommon dependence on a modality-specic semanticsubsystem the observation that these same categoriescan be damaged independently of each other poses aserious threat to the theory That is in the measure towhich one is committed to explaining the observedco-occurrence of impairment of for example the cate-gories of animals and of fruits and vegetables as reect-ing their shared dependence on the hypothesized visualsemantic subsystem one is thereby committed to theirnecessary co-occurrence and their dissociation wouldconstitute evidence against the hypothesized semanticsubsystem

Warrington and McCarthy (1987) were keenly awareof this danger to the SFT and tried to deal with it byhypothesizing further subdivisions within the visual se-mantic subsystem They argued that the dissociation ofdecits of the categories of animals and of fruits andvegetables may be explained by assuming that someperceptual features are more important for animals thanfor fruits and vegetables and vice versa for some otherperceptual features They speculated that shape may be

more important for the categories of owers and animalsand that color may be more important for the categoryof fruits and vegetables And presumably in order toexplain the other patterns of dissociations of category-specic decits (eg animals from owers animals frommusical instruments) further subdivisions would have tobe specied within the visual and functional semanticsubsystems However no independent evidence hasbeen provided for the claim that distinction amongmembers of different semantic categories depend differ-entially on color shape or other sensory features Norhas it been shown that impairment of particular seman-tic categories is associated with special difculties forspecic types of sensory information (eg greater dif-culty processing color in patients with selective damageto the categories of fruits and vegetables) Furthermoreit should be noted that the more subdivisions one pro-poses specically in order to accommodate dissocia-tions of particular categories the more this proposalbecomes indistinguishable from a categorical account ofcategory-specic decits

The evidence and arguments presented in this sectionhave shown that one of the pillars of the SFT does nothold Contrary to the early reports of category-specicdecits that stressed the co-occurrence of conceptuallydisparate combinations of categories (eg animals foodsand musical instruments) there are a number of well-documented cases of dissociations of these categoriesAnd as we have seen there appears to be no clearlymotivated basis for the argument that attested patternsof associations and dissociations of semantic categorydecits are readily explicable in terms of selective dam-age to modality-specic semantic subsystems These criti-cisms of the SFT undermine its supposed superiorityover categorical accounts in explaining the occurrenceof category-specic decits We turn now to the othermajor argument for the SFTmdashthe claim that patientswith selective damage to the living category are dispro-portionately impaired in processing their visual proper-ties

Is Knowledge of Visual Properties More SeverelyImpaired Than Knowledge of Functional Propertiesin Individuals with Category-Specic Decits forLiving Things

The claim that semantic category-specic decits reectselective damage to the visual or to the functional8

semantic subsystems predicts that subjects with selec-tive damage to the living or the nonliving categoriesshould show disproportionate difculty with visual orfunctional properties respectively This expectation isderived not only from Warrington Shallice andMcCarthyrsquos theory (Warrington amp McCarthy 1983 1987Warrington amp Shallice 1984) of the semantic system butalso from the computational variant proposed by Farah

Caramazza and Shelton 5

and McClelland (1991) The results of several studieshave been interpreted as having conrmed this predic-tion That is there are reports of subjects with dispropor-tionate impairment of the category of living things whoare also supposedly disproportionately impaired in proc-essing the visual attributes of living things

The rst studies that explicitly addressed the possibil-ity of a co-occurrence of category- and modality-specicsemantic decits are those of Basso et al (1988) Sartoriand Job (1988)9 and Silveri and Gainotti (1988) In allthree studies it was reported that subjects with dispro-portionate difculty with living things also had dispro-portionate difculty responding to questions about thevisual attributes of living objects For example Basso etal report that their subject (NV) correctly answered 25of 29 questions about the functional attributes of livingthings (eg Does it live in Italy or in the desert) butonly 10 of 20 questions about their sensory attributes(eg Does it have a smooth back or is it humpbacked)Similarly subject LA (Silveri amp Gainotti 1988) was onlyable to name 1 of 11 animals in response to denitionsthat stressed visual attributes (eg a black and whitestriped wild horse) but could name 8 of 14 animals inresponse to denitions that stressed functional attributes(eg the king of the jungle)

Later studies also purportedly showed an associationof category- and modality-specic semantic decits (DeRenzi amp Lucchelli 1994 Farah et al 1989 Gainotti ampSilveri 1996 Hart amp Gordon 1992) Thus for exampleFarah et al report that their subject LH was dispropor-tionately impaired in answering questions about visualattributes of living things (eg Do ducks have long earsvs Is peacock served in French restaurants) And DeRenzi and Lucchelli report that their subject Felicia wassignicantly worse at answering questions about physi-cal than ldquofunctional-encyclopedicrdquo attributes of livingthings but that she showed no such difference for non-living things

Despite the seeming convergence of results in favorof the possibility that category-specic decits are alsomodality-specic there are reasons for skepticism ininterpreting these results First there are issues concern-ing the validity of the reported results in each of thestudies cited second there is growing evidence thatcategory-specic decits are not associated with dispro-portionate difculties in processing either the visual orthe functional attributes of objects

Interpretation of some of the studies purporting toshow that patients with category-specic decits forliving things are also disproportionately impaired inprocessing these objectsrsquo visual attributes is underminedby the fact that these studies failed to control the relativedifculty of visual and functional attribute judgmentsStewart et al (1992 Exp 5) have shown that judgmentsabout the visual properties of living things are moredifcult to evaluate than judgments about functionalproperties They have also shown that the disproportion-

ate difculty for visual attributes for living things in apatient with a putative category-specic decit disap-pears when visual and functional judgments are matchedfor difculty (Exp 6) In light of these results it is notpossible to meaningfully interpret some of the earlystudies claiming to show a co-occurrence of category-and modality-specic decits where no attempt wasmade to control the relative difculty of visual and func-tional attribute judgments (eg Basso et al 1988 Sartoriamp Job 1988 Silveri amp Gainotti 198810)

A related difculty is encountered by De Renzi andLucchellirsquos (1994) study Although the authors were ableto show that their subject Felicia was more severelyimpaired in processing visual attributes of living thannonliving category items she was also impaired in proc-essing functional attributes of living things as indicatedfor example by her performance in deciding whether ananimal was native of Italy (only 73 correct) Further-more since no attempt was made to equate visual andfunctional judgments for difculty it is not possible todirectly compare relative performance for the two typesof judgments

Farah et al (1989) argued that their subject LHpresented with a category-specic decit for the livingcategory that was also modality-specic for visual prop-erties However inspection of their data (Table 1 Farahet al) shows that normal subjects were also dispropor-tionately poor in answering questions about the visualproperties of the living category Thus no meaningfulconclusion concerning category-specic decits is pos-sible from this study

Recently Gainotti and Silveri (1996) retested theirsubject LA with new materials designed to be free ofthe methodological problems encountered by their ear-lier report They again showed that LA performed dis-proportionately poorly on tasks involving the processingof visual attributes of living things For example in a taskrequiring the identication of the visual feature onwhich two objects differed they found that LA per-formed worse with animals (15 correct) than artifacts(50 correct) However the two categories were alsosignicantly different in familiarity (on a scale of 1 to 5255 and 396 for animals and artifacts respectively) Andin a color feature naming task in which LA again per-formed more poorly with living than nonliving thingsthere too the two categories differed in familiarity Thusthe interpretation of LArsquos performance regarding theputative association of category- and modality-specicdecits remains problematic at best

Finally Hart and Gordon (1992) have also argued fora modality-specic organization of the semantic systemon the basis of the performance of their subject KRwho presented with a category-specic decit restrictedto animals KR performed very poorly in naming ani-mals (18 of 61) despite being perfectly normal in namingother objects (348 of 350) The striking feature of thissubject was that she could answer correctly all ques-

6 Journal of Cognitive Neuroscience Volume 10 Number 1

tions about functional attributes of animals as well as allquestions about both visual and functional attributes ofinanimate objects but was quite poor in answering ques-tions about the visual attributes of animals Thus thiscase would seem to represent the perfect dissociation insupport of the SFT11 However there are aspects of thissubjectrsquos performance that are problematic for the SFTand there are other features of her performance that mayundermine its usefulness altogether

The fact that KR was impaired in processing thevisual properties of only animals is inconsistent with theSFT The theory predicts that damage to visual semanticswould differentially affect the living and nonliving cate-gories It does not predict that it would lead to damageto only the category of animals At the very least itpredicts impairment of other living things (eg fruits)besides animals as well as less-marked impairment of thenonliving category None of these conditions were metby the results of this study Equally problematic for theSFT is the fact that KRrsquos decit in processing visualproperties of animals was restricted to language inputsShe only performed poorly with visual attributes whenshe was required to respond to verbal inputs or torespond verbally Thus for example she performed per-fectly in distinguishing between appropriately and inap-propriately colored animals but could not perform thesame discrimination when the color alternatives weregiven verbally This result is also highly problematic forthe SFT The theory predicts equal difculties (barringadditional sensory or language decits) for visual andverbal tasks because damage to the visual semantic sub-system would presumably lead to impairments in alltasks involving the use of this system Thus KRrsquos selec-tive difculty for visual properties restricted to the ver-bal domain is uninterpretable within the SFT

Perhaps most problematic about the Hart and Gordon(1992) study is their subjectrsquos performance in a forced-choice property judgment task In this task KR wasrequired to choose between two visual or two nonphysi-cal properties of animals (eg Is an elephant orange orgray or Is an elephant a food or an animal) The prop-erties were chosen in such a way that they includedproperties that she had produced correctly and incor-rectly in a previous direct recall task (eg Whatrsquos thecolor of lemon Yellow Whatrsquos the color of an elephantOrange) In this task she virtually always (186 of 187)picked the choice corresponding to the property shehad produced in the previously administered propertynaming task whether correct or incorrect Thus forexample consistent with her response in the propertyproduction task she chose orange when given thechoice Is an elephant orange or gray She chose theincorrect strange response in 54 out of 55 trials Theunexpected systematicity of KRrsquos strange errors raisesquestions about the usefulness of this study for inform-ing theories of normal language because it appears thatshe may have come to have systematic ldquostrange beliefsrdquo

about some animals12 Nevertheless the most that canbe concluded for the SFT from the Hart and Gordonstudy is that those aspects of KRrsquos performance that arenot strange are not explicable within the theory

This review of the experimental evidence cited insupport of the claim that subjects with a category-specic decit for living things are disproportionatelyimpaired in processing the visual features of conceptshas shown it to be inadequate for the stated purpose Ineach case (with the exception of Hart and Gordon 1992but there are other problems with this study) the failureto adequately control for differential levels of difcultyin processing visual versus functional properties of con-cepts undermines the possibility of drawing clear infer-ences from the results13 Thus there is no compellingempirical evidence in favor of the claim that category-specic decits are also necessarily modality-specicdecits Furthermore there is growing evidence thatsubjects with category-specic decits for living thingsare equally impaired in processing visual and functionalattributes of objectsmdashevidence that is directly in conictwith the SFT

Laiacona Barbarotto amp Capitani (1993) and Laiaconaet al (1997) have provided the clearest evidence to datefor equal levels of impairment for visual and functionalattributes in cases of category-specic decit for livingthings In the earlier of the two studies they reportedtwo trauma cases FM and GR with disproportionateimpairment in processing living things (FM 20 vs 70correct naming of living and nonliving things respec-tively GR 13 vs 73 correct naming of living andnonliving things respectively) When these subjectswere tested in a forced-choice task with strictly matchedquestions about visual or functional properties of ob-jects (Laiacona Barbarotto Trivelli amp Capitani 1993)they performed equally poorly with the two types ofattributes Thus FM responded correctly 73 and 69of the time to questions about visual and functionalproperties of living things respectively and he re-sponded correctly 96 of the time to both visual andfunctional properties of nonliving things Similarly GRresponded correctly 55 and 58 of the time to ques-tions about visual and functional properties of livingthings respectively and he responded correctly 91 ofthe time to visual properties and 84 of the time tofunctional properties of nonliving things In a more re-cent study Laiacona et al (1997) again observed equallevels of impairment for knowledge of visual and func-tional attributes in two new cases of category-specicdecit for living things14

Two other studies (Funnell amp De Mornay Davies 1997Sheridan amp Humphreys 1993) further conrm this pat-tern of results Sheridan and Humphreys reported a sub-ject with a category-specic decit for living things whowas equally impaired with visual and functional attributejudgments (14 of 20 and 13 of 20 for visual and func-tional attributes of animals respectively) And in a new

Caramazza and Shelton 7

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

whether it is reasonable to assume that the observedassociations of category-specic decits reect the or-ganizing principle of modality-specic semantics Thuswhat underlying sensoryfunctional principles wouldgroup together the categories of animals foods andmusical instruments versus the categories of furnituretools and body parts The mere assertion that the mean-ings of the items in the rst set are more dependent onvisual or other sensory attributes and those of the sec-ond set are more dependent on functional attributes isnot particularly convincing Consider for example thecontrast among carrot celery apple orange avocadotomato hamburger scrambled eggs pasta beer and wineThese items are clearly visually different from one an-other but they are also functionally different One mightgo so far as to contend that what is important fordiscriminating among them is not so much their visualshape but their functions used to make juice used fordessert eaten at breakfast Italian food fast food eatenraw eaten cooked used for minestrone and so on Thesame argument can be made for musical instrumentswith respect to the importance of their functional prop-erties And certainly visual shape is as important fordistinguishing hands heads beds stools hammers andscrewdrivers as is their function Nonetheless the claimthat the relative ldquoweightingrdquo of the sensory and func-tional properties for discriminating among members ofa semantic category provides the binding factor for someof the observed associations of category-specic decitshas never been developed in enough detail to allowserious consideration of its merits7

Far more damaging to the SFT is the pattern of disso-ciations of category-specic decits Since part of themotivation for the SFT is the claim that certain semanticcategories tend to be damaged together because of theircommon dependence on a modality-specic semanticsubsystem the observation that these same categoriescan be damaged independently of each other poses aserious threat to the theory That is in the measure towhich one is committed to explaining the observedco-occurrence of impairment of for example the cate-gories of animals and of fruits and vegetables as reect-ing their shared dependence on the hypothesized visualsemantic subsystem one is thereby committed to theirnecessary co-occurrence and their dissociation wouldconstitute evidence against the hypothesized semanticsubsystem

Warrington and McCarthy (1987) were keenly awareof this danger to the SFT and tried to deal with it byhypothesizing further subdivisions within the visual se-mantic subsystem They argued that the dissociation ofdecits of the categories of animals and of fruits andvegetables may be explained by assuming that someperceptual features are more important for animals thanfor fruits and vegetables and vice versa for some otherperceptual features They speculated that shape may be

more important for the categories of owers and animalsand that color may be more important for the categoryof fruits and vegetables And presumably in order toexplain the other patterns of dissociations of category-specic decits (eg animals from owers animals frommusical instruments) further subdivisions would have tobe specied within the visual and functional semanticsubsystems However no independent evidence hasbeen provided for the claim that distinction amongmembers of different semantic categories depend differ-entially on color shape or other sensory features Norhas it been shown that impairment of particular seman-tic categories is associated with special difculties forspecic types of sensory information (eg greater dif-culty processing color in patients with selective damageto the categories of fruits and vegetables) Furthermoreit should be noted that the more subdivisions one pro-poses specically in order to accommodate dissocia-tions of particular categories the more this proposalbecomes indistinguishable from a categorical account ofcategory-specic decits

The evidence and arguments presented in this sectionhave shown that one of the pillars of the SFT does nothold Contrary to the early reports of category-specicdecits that stressed the co-occurrence of conceptuallydisparate combinations of categories (eg animals foodsand musical instruments) there are a number of well-documented cases of dissociations of these categoriesAnd as we have seen there appears to be no clearlymotivated basis for the argument that attested patternsof associations and dissociations of semantic categorydecits are readily explicable in terms of selective dam-age to modality-specic semantic subsystems These criti-cisms of the SFT undermine its supposed superiorityover categorical accounts in explaining the occurrenceof category-specic decits We turn now to the othermajor argument for the SFTmdashthe claim that patientswith selective damage to the living category are dispro-portionately impaired in processing their visual proper-ties

Is Knowledge of Visual Properties More SeverelyImpaired Than Knowledge of Functional Propertiesin Individuals with Category-Specic Decits forLiving Things

The claim that semantic category-specic decits reectselective damage to the visual or to the functional8

semantic subsystems predicts that subjects with selec-tive damage to the living or the nonliving categoriesshould show disproportionate difculty with visual orfunctional properties respectively This expectation isderived not only from Warrington Shallice andMcCarthyrsquos theory (Warrington amp McCarthy 1983 1987Warrington amp Shallice 1984) of the semantic system butalso from the computational variant proposed by Farah

Caramazza and Shelton 5

and McClelland (1991) The results of several studieshave been interpreted as having conrmed this predic-tion That is there are reports of subjects with dispropor-tionate impairment of the category of living things whoare also supposedly disproportionately impaired in proc-essing the visual attributes of living things

The rst studies that explicitly addressed the possibil-ity of a co-occurrence of category- and modality-specicsemantic decits are those of Basso et al (1988) Sartoriand Job (1988)9 and Silveri and Gainotti (1988) In allthree studies it was reported that subjects with dispro-portionate difculty with living things also had dispro-portionate difculty responding to questions about thevisual attributes of living objects For example Basso etal report that their subject (NV) correctly answered 25of 29 questions about the functional attributes of livingthings (eg Does it live in Italy or in the desert) butonly 10 of 20 questions about their sensory attributes(eg Does it have a smooth back or is it humpbacked)Similarly subject LA (Silveri amp Gainotti 1988) was onlyable to name 1 of 11 animals in response to denitionsthat stressed visual attributes (eg a black and whitestriped wild horse) but could name 8 of 14 animals inresponse to denitions that stressed functional attributes(eg the king of the jungle)

Later studies also purportedly showed an associationof category- and modality-specic semantic decits (DeRenzi amp Lucchelli 1994 Farah et al 1989 Gainotti ampSilveri 1996 Hart amp Gordon 1992) Thus for exampleFarah et al report that their subject LH was dispropor-tionately impaired in answering questions about visualattributes of living things (eg Do ducks have long earsvs Is peacock served in French restaurants) And DeRenzi and Lucchelli report that their subject Felicia wassignicantly worse at answering questions about physi-cal than ldquofunctional-encyclopedicrdquo attributes of livingthings but that she showed no such difference for non-living things

Despite the seeming convergence of results in favorof the possibility that category-specic decits are alsomodality-specic there are reasons for skepticism ininterpreting these results First there are issues concern-ing the validity of the reported results in each of thestudies cited second there is growing evidence thatcategory-specic decits are not associated with dispro-portionate difculties in processing either the visual orthe functional attributes of objects

Interpretation of some of the studies purporting toshow that patients with category-specic decits forliving things are also disproportionately impaired inprocessing these objectsrsquo visual attributes is underminedby the fact that these studies failed to control the relativedifculty of visual and functional attribute judgmentsStewart et al (1992 Exp 5) have shown that judgmentsabout the visual properties of living things are moredifcult to evaluate than judgments about functionalproperties They have also shown that the disproportion-

ate difculty for visual attributes for living things in apatient with a putative category-specic decit disap-pears when visual and functional judgments are matchedfor difculty (Exp 6) In light of these results it is notpossible to meaningfully interpret some of the earlystudies claiming to show a co-occurrence of category-and modality-specic decits where no attempt wasmade to control the relative difculty of visual and func-tional attribute judgments (eg Basso et al 1988 Sartoriamp Job 1988 Silveri amp Gainotti 198810)

A related difculty is encountered by De Renzi andLucchellirsquos (1994) study Although the authors were ableto show that their subject Felicia was more severelyimpaired in processing visual attributes of living thannonliving category items she was also impaired in proc-essing functional attributes of living things as indicatedfor example by her performance in deciding whether ananimal was native of Italy (only 73 correct) Further-more since no attempt was made to equate visual andfunctional judgments for difculty it is not possible todirectly compare relative performance for the two typesof judgments

Farah et al (1989) argued that their subject LHpresented with a category-specic decit for the livingcategory that was also modality-specic for visual prop-erties However inspection of their data (Table 1 Farahet al) shows that normal subjects were also dispropor-tionately poor in answering questions about the visualproperties of the living category Thus no meaningfulconclusion concerning category-specic decits is pos-sible from this study

Recently Gainotti and Silveri (1996) retested theirsubject LA with new materials designed to be free ofthe methodological problems encountered by their ear-lier report They again showed that LA performed dis-proportionately poorly on tasks involving the processingof visual attributes of living things For example in a taskrequiring the identication of the visual feature onwhich two objects differed they found that LA per-formed worse with animals (15 correct) than artifacts(50 correct) However the two categories were alsosignicantly different in familiarity (on a scale of 1 to 5255 and 396 for animals and artifacts respectively) Andin a color feature naming task in which LA again per-formed more poorly with living than nonliving thingsthere too the two categories differed in familiarity Thusthe interpretation of LArsquos performance regarding theputative association of category- and modality-specicdecits remains problematic at best

Finally Hart and Gordon (1992) have also argued fora modality-specic organization of the semantic systemon the basis of the performance of their subject KRwho presented with a category-specic decit restrictedto animals KR performed very poorly in naming ani-mals (18 of 61) despite being perfectly normal in namingother objects (348 of 350) The striking feature of thissubject was that she could answer correctly all ques-

6 Journal of Cognitive Neuroscience Volume 10 Number 1

tions about functional attributes of animals as well as allquestions about both visual and functional attributes ofinanimate objects but was quite poor in answering ques-tions about the visual attributes of animals Thus thiscase would seem to represent the perfect dissociation insupport of the SFT11 However there are aspects of thissubjectrsquos performance that are problematic for the SFTand there are other features of her performance that mayundermine its usefulness altogether

The fact that KR was impaired in processing thevisual properties of only animals is inconsistent with theSFT The theory predicts that damage to visual semanticswould differentially affect the living and nonliving cate-gories It does not predict that it would lead to damageto only the category of animals At the very least itpredicts impairment of other living things (eg fruits)besides animals as well as less-marked impairment of thenonliving category None of these conditions were metby the results of this study Equally problematic for theSFT is the fact that KRrsquos decit in processing visualproperties of animals was restricted to language inputsShe only performed poorly with visual attributes whenshe was required to respond to verbal inputs or torespond verbally Thus for example she performed per-fectly in distinguishing between appropriately and inap-propriately colored animals but could not perform thesame discrimination when the color alternatives weregiven verbally This result is also highly problematic forthe SFT The theory predicts equal difculties (barringadditional sensory or language decits) for visual andverbal tasks because damage to the visual semantic sub-system would presumably lead to impairments in alltasks involving the use of this system Thus KRrsquos selec-tive difculty for visual properties restricted to the ver-bal domain is uninterpretable within the SFT

Perhaps most problematic about the Hart and Gordon(1992) study is their subjectrsquos performance in a forced-choice property judgment task In this task KR wasrequired to choose between two visual or two nonphysi-cal properties of animals (eg Is an elephant orange orgray or Is an elephant a food or an animal) The prop-erties were chosen in such a way that they includedproperties that she had produced correctly and incor-rectly in a previous direct recall task (eg Whatrsquos thecolor of lemon Yellow Whatrsquos the color of an elephantOrange) In this task she virtually always (186 of 187)picked the choice corresponding to the property shehad produced in the previously administered propertynaming task whether correct or incorrect Thus forexample consistent with her response in the propertyproduction task she chose orange when given thechoice Is an elephant orange or gray She chose theincorrect strange response in 54 out of 55 trials Theunexpected systematicity of KRrsquos strange errors raisesquestions about the usefulness of this study for inform-ing theories of normal language because it appears thatshe may have come to have systematic ldquostrange beliefsrdquo

about some animals12 Nevertheless the most that canbe concluded for the SFT from the Hart and Gordonstudy is that those aspects of KRrsquos performance that arenot strange are not explicable within the theory

This review of the experimental evidence cited insupport of the claim that subjects with a category-specic decit for living things are disproportionatelyimpaired in processing the visual features of conceptshas shown it to be inadequate for the stated purpose Ineach case (with the exception of Hart and Gordon 1992but there are other problems with this study) the failureto adequately control for differential levels of difcultyin processing visual versus functional properties of con-cepts undermines the possibility of drawing clear infer-ences from the results13 Thus there is no compellingempirical evidence in favor of the claim that category-specic decits are also necessarily modality-specicdecits Furthermore there is growing evidence thatsubjects with category-specic decits for living thingsare equally impaired in processing visual and functionalattributes of objectsmdashevidence that is directly in conictwith the SFT

Laiacona Barbarotto amp Capitani (1993) and Laiaconaet al (1997) have provided the clearest evidence to datefor equal levels of impairment for visual and functionalattributes in cases of category-specic decit for livingthings In the earlier of the two studies they reportedtwo trauma cases FM and GR with disproportionateimpairment in processing living things (FM 20 vs 70correct naming of living and nonliving things respec-tively GR 13 vs 73 correct naming of living andnonliving things respectively) When these subjectswere tested in a forced-choice task with strictly matchedquestions about visual or functional properties of ob-jects (Laiacona Barbarotto Trivelli amp Capitani 1993)they performed equally poorly with the two types ofattributes Thus FM responded correctly 73 and 69of the time to questions about visual and functionalproperties of living things respectively and he re-sponded correctly 96 of the time to both visual andfunctional properties of nonliving things Similarly GRresponded correctly 55 and 58 of the time to ques-tions about visual and functional properties of livingthings respectively and he responded correctly 91 ofthe time to visual properties and 84 of the time tofunctional properties of nonliving things In a more re-cent study Laiacona et al (1997) again observed equallevels of impairment for knowledge of visual and func-tional attributes in two new cases of category-specicdecit for living things14

Two other studies (Funnell amp De Mornay Davies 1997Sheridan amp Humphreys 1993) further conrm this pat-tern of results Sheridan and Humphreys reported a sub-ject with a category-specic decit for living things whowas equally impaired with visual and functional attributejudgments (14 of 20 and 13 of 20 for visual and func-tional attributes of animals respectively) And in a new

Caramazza and Shelton 7

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

and McClelland (1991) The results of several studieshave been interpreted as having conrmed this predic-tion That is there are reports of subjects with dispropor-tionate impairment of the category of living things whoare also supposedly disproportionately impaired in proc-essing the visual attributes of living things

The rst studies that explicitly addressed the possibil-ity of a co-occurrence of category- and modality-specicsemantic decits are those of Basso et al (1988) Sartoriand Job (1988)9 and Silveri and Gainotti (1988) In allthree studies it was reported that subjects with dispro-portionate difculty with living things also had dispro-portionate difculty responding to questions about thevisual attributes of living objects For example Basso etal report that their subject (NV) correctly answered 25of 29 questions about the functional attributes of livingthings (eg Does it live in Italy or in the desert) butonly 10 of 20 questions about their sensory attributes(eg Does it have a smooth back or is it humpbacked)Similarly subject LA (Silveri amp Gainotti 1988) was onlyable to name 1 of 11 animals in response to denitionsthat stressed visual attributes (eg a black and whitestriped wild horse) but could name 8 of 14 animals inresponse to denitions that stressed functional attributes(eg the king of the jungle)

Later studies also purportedly showed an associationof category- and modality-specic semantic decits (DeRenzi amp Lucchelli 1994 Farah et al 1989 Gainotti ampSilveri 1996 Hart amp Gordon 1992) Thus for exampleFarah et al report that their subject LH was dispropor-tionately impaired in answering questions about visualattributes of living things (eg Do ducks have long earsvs Is peacock served in French restaurants) And DeRenzi and Lucchelli report that their subject Felicia wassignicantly worse at answering questions about physi-cal than ldquofunctional-encyclopedicrdquo attributes of livingthings but that she showed no such difference for non-living things

Despite the seeming convergence of results in favorof the possibility that category-specic decits are alsomodality-specic there are reasons for skepticism ininterpreting these results First there are issues concern-ing the validity of the reported results in each of thestudies cited second there is growing evidence thatcategory-specic decits are not associated with dispro-portionate difculties in processing either the visual orthe functional attributes of objects

Interpretation of some of the studies purporting toshow that patients with category-specic decits forliving things are also disproportionately impaired inprocessing these objectsrsquo visual attributes is underminedby the fact that these studies failed to control the relativedifculty of visual and functional attribute judgmentsStewart et al (1992 Exp 5) have shown that judgmentsabout the visual properties of living things are moredifcult to evaluate than judgments about functionalproperties They have also shown that the disproportion-

ate difculty for visual attributes for living things in apatient with a putative category-specic decit disap-pears when visual and functional judgments are matchedfor difculty (Exp 6) In light of these results it is notpossible to meaningfully interpret some of the earlystudies claiming to show a co-occurrence of category-and modality-specic decits where no attempt wasmade to control the relative difculty of visual and func-tional attribute judgments (eg Basso et al 1988 Sartoriamp Job 1988 Silveri amp Gainotti 198810)

A related difculty is encountered by De Renzi andLucchellirsquos (1994) study Although the authors were ableto show that their subject Felicia was more severelyimpaired in processing visual attributes of living thannonliving category items she was also impaired in proc-essing functional attributes of living things as indicatedfor example by her performance in deciding whether ananimal was native of Italy (only 73 correct) Further-more since no attempt was made to equate visual andfunctional judgments for difculty it is not possible todirectly compare relative performance for the two typesof judgments

Farah et al (1989) argued that their subject LHpresented with a category-specic decit for the livingcategory that was also modality-specic for visual prop-erties However inspection of their data (Table 1 Farahet al) shows that normal subjects were also dispropor-tionately poor in answering questions about the visualproperties of the living category Thus no meaningfulconclusion concerning category-specic decits is pos-sible from this study

Recently Gainotti and Silveri (1996) retested theirsubject LA with new materials designed to be free ofthe methodological problems encountered by their ear-lier report They again showed that LA performed dis-proportionately poorly on tasks involving the processingof visual attributes of living things For example in a taskrequiring the identication of the visual feature onwhich two objects differed they found that LA per-formed worse with animals (15 correct) than artifacts(50 correct) However the two categories were alsosignicantly different in familiarity (on a scale of 1 to 5255 and 396 for animals and artifacts respectively) Andin a color feature naming task in which LA again per-formed more poorly with living than nonliving thingsthere too the two categories differed in familiarity Thusthe interpretation of LArsquos performance regarding theputative association of category- and modality-specicdecits remains problematic at best

Finally Hart and Gordon (1992) have also argued fora modality-specic organization of the semantic systemon the basis of the performance of their subject KRwho presented with a category-specic decit restrictedto animals KR performed very poorly in naming ani-mals (18 of 61) despite being perfectly normal in namingother objects (348 of 350) The striking feature of thissubject was that she could answer correctly all ques-

6 Journal of Cognitive Neuroscience Volume 10 Number 1

tions about functional attributes of animals as well as allquestions about both visual and functional attributes ofinanimate objects but was quite poor in answering ques-tions about the visual attributes of animals Thus thiscase would seem to represent the perfect dissociation insupport of the SFT11 However there are aspects of thissubjectrsquos performance that are problematic for the SFTand there are other features of her performance that mayundermine its usefulness altogether

The fact that KR was impaired in processing thevisual properties of only animals is inconsistent with theSFT The theory predicts that damage to visual semanticswould differentially affect the living and nonliving cate-gories It does not predict that it would lead to damageto only the category of animals At the very least itpredicts impairment of other living things (eg fruits)besides animals as well as less-marked impairment of thenonliving category None of these conditions were metby the results of this study Equally problematic for theSFT is the fact that KRrsquos decit in processing visualproperties of animals was restricted to language inputsShe only performed poorly with visual attributes whenshe was required to respond to verbal inputs or torespond verbally Thus for example she performed per-fectly in distinguishing between appropriately and inap-propriately colored animals but could not perform thesame discrimination when the color alternatives weregiven verbally This result is also highly problematic forthe SFT The theory predicts equal difculties (barringadditional sensory or language decits) for visual andverbal tasks because damage to the visual semantic sub-system would presumably lead to impairments in alltasks involving the use of this system Thus KRrsquos selec-tive difculty for visual properties restricted to the ver-bal domain is uninterpretable within the SFT

Perhaps most problematic about the Hart and Gordon(1992) study is their subjectrsquos performance in a forced-choice property judgment task In this task KR wasrequired to choose between two visual or two nonphysi-cal properties of animals (eg Is an elephant orange orgray or Is an elephant a food or an animal) The prop-erties were chosen in such a way that they includedproperties that she had produced correctly and incor-rectly in a previous direct recall task (eg Whatrsquos thecolor of lemon Yellow Whatrsquos the color of an elephantOrange) In this task she virtually always (186 of 187)picked the choice corresponding to the property shehad produced in the previously administered propertynaming task whether correct or incorrect Thus forexample consistent with her response in the propertyproduction task she chose orange when given thechoice Is an elephant orange or gray She chose theincorrect strange response in 54 out of 55 trials Theunexpected systematicity of KRrsquos strange errors raisesquestions about the usefulness of this study for inform-ing theories of normal language because it appears thatshe may have come to have systematic ldquostrange beliefsrdquo

about some animals12 Nevertheless the most that canbe concluded for the SFT from the Hart and Gordonstudy is that those aspects of KRrsquos performance that arenot strange are not explicable within the theory

This review of the experimental evidence cited insupport of the claim that subjects with a category-specic decit for living things are disproportionatelyimpaired in processing the visual features of conceptshas shown it to be inadequate for the stated purpose Ineach case (with the exception of Hart and Gordon 1992but there are other problems with this study) the failureto adequately control for differential levels of difcultyin processing visual versus functional properties of con-cepts undermines the possibility of drawing clear infer-ences from the results13 Thus there is no compellingempirical evidence in favor of the claim that category-specic decits are also necessarily modality-specicdecits Furthermore there is growing evidence thatsubjects with category-specic decits for living thingsare equally impaired in processing visual and functionalattributes of objectsmdashevidence that is directly in conictwith the SFT

Laiacona Barbarotto amp Capitani (1993) and Laiaconaet al (1997) have provided the clearest evidence to datefor equal levels of impairment for visual and functionalattributes in cases of category-specic decit for livingthings In the earlier of the two studies they reportedtwo trauma cases FM and GR with disproportionateimpairment in processing living things (FM 20 vs 70correct naming of living and nonliving things respec-tively GR 13 vs 73 correct naming of living andnonliving things respectively) When these subjectswere tested in a forced-choice task with strictly matchedquestions about visual or functional properties of ob-jects (Laiacona Barbarotto Trivelli amp Capitani 1993)they performed equally poorly with the two types ofattributes Thus FM responded correctly 73 and 69of the time to questions about visual and functionalproperties of living things respectively and he re-sponded correctly 96 of the time to both visual andfunctional properties of nonliving things Similarly GRresponded correctly 55 and 58 of the time to ques-tions about visual and functional properties of livingthings respectively and he responded correctly 91 ofthe time to visual properties and 84 of the time tofunctional properties of nonliving things In a more re-cent study Laiacona et al (1997) again observed equallevels of impairment for knowledge of visual and func-tional attributes in two new cases of category-specicdecit for living things14

Two other studies (Funnell amp De Mornay Davies 1997Sheridan amp Humphreys 1993) further conrm this pat-tern of results Sheridan and Humphreys reported a sub-ject with a category-specic decit for living things whowas equally impaired with visual and functional attributejudgments (14 of 20 and 13 of 20 for visual and func-tional attributes of animals respectively) And in a new

Caramazza and Shelton 7

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

tions about functional attributes of animals as well as allquestions about both visual and functional attributes ofinanimate objects but was quite poor in answering ques-tions about the visual attributes of animals Thus thiscase would seem to represent the perfect dissociation insupport of the SFT11 However there are aspects of thissubjectrsquos performance that are problematic for the SFTand there are other features of her performance that mayundermine its usefulness altogether

The fact that KR was impaired in processing thevisual properties of only animals is inconsistent with theSFT The theory predicts that damage to visual semanticswould differentially affect the living and nonliving cate-gories It does not predict that it would lead to damageto only the category of animals At the very least itpredicts impairment of other living things (eg fruits)besides animals as well as less-marked impairment of thenonliving category None of these conditions were metby the results of this study Equally problematic for theSFT is the fact that KRrsquos decit in processing visualproperties of animals was restricted to language inputsShe only performed poorly with visual attributes whenshe was required to respond to verbal inputs or torespond verbally Thus for example she performed per-fectly in distinguishing between appropriately and inap-propriately colored animals but could not perform thesame discrimination when the color alternatives weregiven verbally This result is also highly problematic forthe SFT The theory predicts equal difculties (barringadditional sensory or language decits) for visual andverbal tasks because damage to the visual semantic sub-system would presumably lead to impairments in alltasks involving the use of this system Thus KRrsquos selec-tive difculty for visual properties restricted to the ver-bal domain is uninterpretable within the SFT

Perhaps most problematic about the Hart and Gordon(1992) study is their subjectrsquos performance in a forced-choice property judgment task In this task KR wasrequired to choose between two visual or two nonphysi-cal properties of animals (eg Is an elephant orange orgray or Is an elephant a food or an animal) The prop-erties were chosen in such a way that they includedproperties that she had produced correctly and incor-rectly in a previous direct recall task (eg Whatrsquos thecolor of lemon Yellow Whatrsquos the color of an elephantOrange) In this task she virtually always (186 of 187)picked the choice corresponding to the property shehad produced in the previously administered propertynaming task whether correct or incorrect Thus forexample consistent with her response in the propertyproduction task she chose orange when given thechoice Is an elephant orange or gray She chose theincorrect strange response in 54 out of 55 trials Theunexpected systematicity of KRrsquos strange errors raisesquestions about the usefulness of this study for inform-ing theories of normal language because it appears thatshe may have come to have systematic ldquostrange beliefsrdquo

about some animals12 Nevertheless the most that canbe concluded for the SFT from the Hart and Gordonstudy is that those aspects of KRrsquos performance that arenot strange are not explicable within the theory

This review of the experimental evidence cited insupport of the claim that subjects with a category-specic decit for living things are disproportionatelyimpaired in processing the visual features of conceptshas shown it to be inadequate for the stated purpose Ineach case (with the exception of Hart and Gordon 1992but there are other problems with this study) the failureto adequately control for differential levels of difcultyin processing visual versus functional properties of con-cepts undermines the possibility of drawing clear infer-ences from the results13 Thus there is no compellingempirical evidence in favor of the claim that category-specic decits are also necessarily modality-specicdecits Furthermore there is growing evidence thatsubjects with category-specic decits for living thingsare equally impaired in processing visual and functionalattributes of objectsmdashevidence that is directly in conictwith the SFT

Laiacona Barbarotto amp Capitani (1993) and Laiaconaet al (1997) have provided the clearest evidence to datefor equal levels of impairment for visual and functionalattributes in cases of category-specic decit for livingthings In the earlier of the two studies they reportedtwo trauma cases FM and GR with disproportionateimpairment in processing living things (FM 20 vs 70correct naming of living and nonliving things respec-tively GR 13 vs 73 correct naming of living andnonliving things respectively) When these subjectswere tested in a forced-choice task with strictly matchedquestions about visual or functional properties of ob-jects (Laiacona Barbarotto Trivelli amp Capitani 1993)they performed equally poorly with the two types ofattributes Thus FM responded correctly 73 and 69of the time to questions about visual and functionalproperties of living things respectively and he re-sponded correctly 96 of the time to both visual andfunctional properties of nonliving things Similarly GRresponded correctly 55 and 58 of the time to ques-tions about visual and functional properties of livingthings respectively and he responded correctly 91 ofthe time to visual properties and 84 of the time tofunctional properties of nonliving things In a more re-cent study Laiacona et al (1997) again observed equallevels of impairment for knowledge of visual and func-tional attributes in two new cases of category-specicdecit for living things14

Two other studies (Funnell amp De Mornay Davies 1997Sheridan amp Humphreys 1993) further conrm this pat-tern of results Sheridan and Humphreys reported a sub-ject with a category-specic decit for living things whowas equally impaired with visual and functional attributejudgments (14 of 20 and 13 of 20 for visual and func-tional attributes of animals respectively) And in a new

Caramazza and Shelton 7

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

analysis of JBR one of the cases of category-specicdecit for living things originally reported by Warringtonand Shallice (1984) Funnell and De Mornay Davies(1997) found that he is equally impaired in verifyingvisual and functional attribute questions about livingthings15 These results indicate that knowledge of visualattributes of living things is not necessarily dispropor-tionately impaired (relative to knowledge of functionalattributes) in subjects with a category-specic decit forliving things Thus the second of the two major predic-tions of the SFT is not conrmed

The Organized Unitary Content Hypothesis(OUCH)

Another class of reductionist hypotheses rejects the mo-dality-specic16 claim of semantic organization proposedby the SFT but also explains category-specic decits asresulting from noncategorical properties of semanticrepresentations The OUCH is one such account(Caramazza Hillis Rapp amp Romani 1990 Hillis Rapp ampCaramazza 1995 Rapp Hillis amp Caramazza 1993 seeRiddoch Humphreys Coltheart amp Funnell 1988 for arelated proposal) This account is based on two funda-mental characteristics of natural kind objects and arti-facts (1) the properties that dene an object (eg dogchair etc) are highly intercorrelated and (2) membersof a superordinate category share many features in com-mon (S Gelman amp Coley 1990 Keil 1989 Markman1989 Rosch 1973 1975 Rosch Mervis Gray Johnson ampBoyes-Braem 1976) Thus for example objects that arecapable of a certain type of bio-mechanical motion (likea dog) tend to have particular types of shapes and to bemade of certain kinds of ldquostuffrdquo (texture color odorsetc) and objects that have a particular shape (like achair) and an inability to move tend to be made ofdifferent kinds of ldquostuffrdquo Furthermore these bundles ofintercorrelated properties are differentially distributed inthe categories of living and nonliving things A conse-quence of the latter property of concepts is that themultidimensional space of semantic properties is nothomogeneously occupied but instead is ldquolumpyrdquomdashthereare regions that are densely packed and others that areonly sparsely occupied17 The denser regions representconcept domains characterized by highly correlatedproperties with the densest regions most likely corre-sponding to natural kind concepts however some arti-facts (eg tools) can also occupy relatively denseregions because they too may share many correlatedproperties (eg shape and function)

One implication of the inhomogeneous nature of theorganization of semantic attributes in the brain is thatfocal damage to the semantic system can result in cate-gory-specic decits This expectation is based on thefollowing reasoning Focal damage to a region of seman-tic space will result in an impairment of those categorieswhose membersrsquo meaning depends on the affected se-

mantic properties and because of the lumpiness of se-mantic space the impairment is likely to be dispropor-tionate for one category or another reecting whichdense region happened to have been damaged Twoother implications follow from the OUCH model One isthat semantic categories with highly correlated proper-ties (ie natural kinds) are more likely to be damaged asa category This expectation follows from the assumptionthat categories with highly correlated properties occupydense regions in semantic space thereby allowing forthe possibility of selective damage to the category Fromthis it follows that natural kinds are more likely to gurein category-specic decits The other prediction thatfollows from OUCH is that various different patterns ofcategory-specic decits are expected to occur reect-ing the vagaries of the distribution of damage to thesemantic space in different cases of brain damage Thatis because in this view the semantic system consists ofa seamless but lumpy space the particular categoriesthat are affected will depend on which specic regionsof the brain are damaged Thus for example OUCH doesnot exclude the possibility of a subject with dispropor-tionate impairment to the category of living thingsfoods musical instruments and precious stones (as wasthe case for JBR reported by Warrington amp Shallice1984)

The other major prediction made by OUCH is thatselective impairment of specic semantic categoriesshould not be associated with disproportionate decitto either visual or functional attributes of objects Thisexpectation is based on the fact that focal damage to thesemantic system should affect closely correlated proper-ties that are likely to involve both visual and functionalattributes This prediction clearly distinguishes theOUCH model from the SFT because as we have seenthe latter theory of conceptual organization predicts theopposite resultmdashnamely that category-specic decitsfor living things should be associated with a dispropor-tionate decit for the visual attributes of objects

The patterns of category-specic decits reviewedhere are consistent with expectations derived fromOUCH The model predicts the occurrence of category-specic decits without postulating a categorical organi-zation of semantic knowledge It also allows for theexistence of various combinations of category-specicdecits And nally it is consistent with the resultsshowing that category-specic decits are not necessar-ily also modality-specic in nature (contrary to the pre-diction derived from the SFT) Thus OUCH offers abetter account than the SFT for the various empiricalphenomena related to category-specic decits

Although OUCH can account for important aspects ofthe category-specic decit phenomenon it is unsatis-factory in at least one respect It is too vague on criticalissues about the nature and organization of semanticinformation allowing it to account for almost any pat-tern of category-specic decits All it needs to do for

8 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

the latter purpose is to assume for example that braindamage has accidentally affected one of the lumpy re-gions of semantic space thereby resulting in a category-specic decit Although this kind of explanatory powerwould be welcome in the context of an explicitly articu-lated theory of semantics in the present case it merelyreects the unconstrained nature of the modelrsquos centralassumptions Furthermore the model fails to provide aprincipled account for the patterns of attested forms ofcategory-specic decits Specically the OUCH (justlike the SFT) fails to explain why it is that by far the mostprevalent form of category-specic decit involves thecategory of living things

Categorical Organization of Knowledge in theBrain A Speculative Hypothesis

The reservations we have voiced about the reductionistaccounts of category-specic decits (the SFT andOUCH models) encourage us to explore the alternativehypothesis that semantic knowledge may be organizedcategorically in the brain (Warrington 1981) The hy-pothesis we wish to entertain is that evolutionary pres-sures have resulted in specialized mechanisms forperceptually and conceptually distinguishing animateand inanimate kinds (R Gelman 1990 Premack 1990)leading to a categorical organization of this knowledgein the brain We will call this hypothesis the domain-specic knowledge hypothesis In the ldquoDiscussionrdquo sec-tion we will elaborate further on this view and offervarious arguments in its defense Here we simply notethat the hypothesis receives initial plausibility from de-velopmental research which has shown that infants asyoung as 3 months old are able to distinguish animatefrom inanimate objects as indicated for example bytheir ability to distinguish biological from nonbiologicalmotion (Bertenthal 1993 Bertenthal Proftt amp Cutting1984) and their ability to distinguish caused from non-caused motion (Leslie 1982 1988 and see Leslie ampKeeble 1987 for results on 6-month-old infants) and thatthe 8- to 10-month-old infantrsquos ability to distinguish ani-mals from nonanimals is unlikely to be merely perceptu-ally based (Quinn amp Eimas 1996) but is most likelyconceptually driven (Mandler 1992) Thus for exam-ple using a dishabituation paradigm Mandler andMcDonough (1993) have shown that 9-month-old infantsdishabituate to an animal after repeatedly seeing modelsof a vehicle (and vice versa) even though the dishabitu-ating stimulus may be highly visually similar to the ha-bituated objects (eg birds and airplanes) Theseobservations further encourage us to explore the possi-bility that a fundamental distinction in human knowl-edgemdashthat between knowledge of animate andinanimate thingsmdashmay be rooted in specic evolution-ary adaptations18

The domain-specic knowledge hypothesis makes thefollowing two predictions about the nature of category-

specic decits First the only ldquotruerdquo category-specicdecits are those involving categories of knowledge forwhich evolutionary pressures have led to the develop-ment of specialized neural mechanisms for their percep-tual and conceptual distinction Plausible categoricaldistinctions are those among animals plant life and arti-facts19 The other major expectation derived from thishypothesis is that (everything else being equal) category-specic decits should result in comparable impair-ments for the visual and functional attributes of aconcept This prediction reects the assumption that thecategory-specic nature of the decit results from thefact that brain damage has affected a categorically organ-ized knowledge system that represents all types of infor-mation relevant to that semantic domain20

The evidence on category-specic decits that wehave reviewed in the preceding sections is consistentwith the expectations derived from the hypothesis thatsemantic knowledge is organized categorically in thebrain although it is also consistent with the OUCHmodel Here we provide further experimental evidencefor the hypothesis that semantic knowledge is organizedcategorically We present a case study of a brain-damagedsubject EW who has a selective decit for the categoryof animals and who is equally impaired for the visual andfunctional attributes of the members of this categoryThis pattern of performancemdashwhich is predicted by thedomain-specic knowledge accountmdashhas not been re-ported previously The results are organized as followsFirst we show that subject EW is disproportionatelyimpaired in naming animals relative to other living thingsand artifacts We then show that this decit is not merelydue to a lexical retrieval problem because EW is alsoseverely impaired in visually recognizing animals and inrecognizing them from their characteristic sounds Thirdwe show that EWrsquos decit occurs at the conceptuallevel because she is not only impaired in processingpictures of animals but also in answering verbal ques-tions about them In this section we also show that herdisproportionate semantic decit for animals is equallysevere for the visual and functional properties of mem-bers of this category

RESULTS

Does EW Have a Category-Specic NamingDecit

Naming the Snodgrass and Vanderwart Pictures

The rst analysis of EWrsquos performance is directed atestablishing that EW has a category-specic namingdecit Naming performance is summarized in Table 1 Aresponse was considered correct if EW provided theSnodgrass and Vanderwart (1980) name or any accept-able response produced by the control subjects (n = 5)For both the control subjects and EW performance isbroken down by animacy and familiarity Familiarity was

Caramazza and Shelton 9

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

divided on the basis of the ratings provided in Snodgrassand Vanderwart where familiarity was rated on a 5-pointscale with 1 being very unfamiliar and 5 being veryfamiliar High-familiarity items were dened as thoseitems with a familiarity rating greater than 25 and low-familiarity items were dened as those items with afamiliarity rating less than or equal to 25 Note that thisis a general breakdown by familiarity and the number ofitems in each cell differs greatly The mean familiarity forhigh-familiarity animate and inanimate items is 322 and373 respectively The mean familiarity for low-familiarityanimate and inanimate items is 202 and 213 respec-tively

Control subjects performed quite well and showed noeffect of either semantic category or familiarity HoweverEW demonstrated signicant difculties naming animalsas compared to nonanimals (z = 811 p lt 005) Althoughshe does demonstrate more difculty naming low-famili-arity items overall (z = 349 p lt 005) note that thelow-familiarity nonanimal items are named at a muchhigher rate than high-familiarity animal items (z = 260p lt 005) This is not the case for the control subjects

EWrsquos performance was not only signicantly differenton animal pictures compared to pictures from manyother semantic categories but the nature of her errorswas qualitatively different as well In the majority (34 of

47) of cases with animals EW either said ldquoI have no ideawhat that isrdquo or produced a semantically related re-sponse (Zebra reg Gorilla I think but Irsquom not sure) Bycontrast she only produced 5 of 137 semantic or ldquodonrsquotknowrdquo responses to items in other semantic categoriesFor the latter categories most of her errors (12 of 137)were semantic descriptions followed by the commentldquoOh what is that calledrdquo Thus for animals she often hadno idea what the correct name of the picture was (ieshe didnrsquot recognize the picture or she named it incor-rectly) whereas for other categories she clearly recog-nized the picture but could not produce the name

Controlling for Nuisance Variables in the NamingTask

As noted in the ldquoIntroductionrdquo it has been shown thatwhen certain stimulus factors are carefully controlledputative cases of category-specic decit may turn outnot to have such a decit after all (eg Stewart et al1992) It is important therefore to carefully control forpossible nuisance factors that may be responsible for asupposed semantic category effect We carried out sev-eral tests to ensure that the noted effect for EW couldnot be ascribed to some such nuisance variable

Table 2 presents an examination of EWrsquos naming

Table 1 Snodgrass and Vanderwart Naming Performance (proportion correct range = correct)

EW Animal Nonanimal

High familiarity 6 of 11 (054) 170 of 181 (094)

Low familiarity 10 of 36 (028) 18 of 22 (081)

Animal Nonanimal

Control subjects Mean Range Mean Range

High familiarity 11 of 11 (10) 11 179 of 181 (099) 177ndash181

Low familiarity 342 of 36 (095) 31ndash36 218 of 22 (099) 21ndash22

Note n = 250 total items Ten items were removed from the set due to lack of consistency in responding by the control subjects(see ldquoMethodsrdquo)

Table 2 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Familiarity and Frequency(proportion correct)

Low familiaritylow frequency Matched familiarity and frequencya

Animals Nonanimals Animals Nonanimals

EW 8 of 24 (033) 16 of 24 (067) 12 of 22 (055) 18 of 22 (082)

Controls 118 of 12 (098) 12 of 12 (10) 11 of 11 (10) 108 of 11 (098)

Range 11ndash12 12 11 10ndash11

Note The items in this analysis were taken from Appendices 2 and 3 in Funnell and Sheridan (1992) They represent items from the Snodgrassand Vanderwart picture set that are either low familiarlow frequency items or are items matched on frequency This was further broken downby animacya Two items in this set (bee amp violin) were removed because they were removed from the entire picture set

10 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

performance on the items included in Funnell and Sheri-danrsquos (1992) tests of naming performance as a functionof animacy and familiarity (from their Appendixes 2 and3) These items are all taken from the Snodgrass andVanderwart picture set The items in the rst set are alllow-familiaritylow-frequency items and the items in thesecond set are matched on familiarity and frequency(ie represent a range of familiarity and frequency)Since the number of items is quite low we have includedEWrsquos naming performance from two administrations ofthe naming task Control subjects only named theSnodgrass and Vanderwart picture set once

It is immediately apparent that EWrsquos naming is af-fected by the animacy variable for both sets of items(z = 292 p lt 005 z = 285 p lt 005 respectively) evenwhen those items have been controlled for familiarityThus taken together with the above analyses EWrsquosdecit in naming animals can be attributed to a decitaffecting the category of animals and not an artifact dueto familiarity of the items

However Stewart et al (1992 see also Gaffan amp Hey-wood 1993) argued that naming could also be inu-enced by visual complexity Table 3 contains EWrsquosnaming performance on a subset of items from theSnodgrass and Vanderwart picture set that are matchedon visual complexity (n = 36) and a subset of items thatare matched (as closely as possible) on both visual com-plexity and familiarity Once again it is obvious that

neither the factor of visual complexity nor the combinedfactor of visual complexity and familiarity is responsiblefor EWrsquos decrement in performance for animate itemsInstead EWrsquos picture-naming performance is inuencedstrongly by the factor of animacy and cannot be ex-plained by extraneous factors such as familiarity or visualcomplexity (z = 575 p lt 005 z = 317 p lt 005respectively)

The Naming Decit Is Restricted to Animals and IsNot General to Living Things

A crucial part of this investigation involves determiningthe boundaries of the category-specic decit Spe-cically we are concerned with determining whetherEW is disproportionately impaired in processing livingthings or the more restricted category of animals Forthis purpose we considered EWrsquos performance for spe-cic semantic categories

Table 4 provides a breakdown of EWrsquos naming per-formance according to specic semantic categories Sev-eral things should be noted First EWrsquos namingperformance is not affected by the category of livingthings but rather by the category of animate thingsThus like several other reported cases (Farah amp Wallace1992 Hart et al 1985 Hillis amp Caramazza 1991) EWrsquosdecit respects a more ne-grained distinction than liv-ingnonliving Although performance broken down by

Table 3 Naming Performance on a Subset of Snodgrass and Vanderwart Pictures Based on Visual Complexity and VisualComplexityFamiliarity (proportion correct)

Matched Complexity Matched Complexity and familiarity

Animals Nonanimals Animals Nonanimals

EW 10 of 36 (028) 32 of 36 (089) 7 of 17 (041) 16 of 17 (094)

Controls 354 of 36 (098) 354 of 36 (098) 166 of 17 (098) 16 of 17 (094)

Range 35ndash36 35ndash36 16ndash17 16ndash17

Note The items in this analysis represent a subset of items from the Snodgrass and Vanderwart picture set that are matched on visual complex-ity (mean = 376 SD = 051) or on visual complexity (mean = 383 SD = 044) and familiarity (animate mean = 278 SD = 084 inanimatemean = 264 SD = 084) This was further broken down by animacy

Table 4 EWrsquos Naming Performance as a Function of Specic Semantic Category (proportion correct)

Category Performance Category Performance

Animal 16 of 47 (034) Kitchenware 16 of 17 (094)

Body part 11 of 12 (092) Musical instrument 8 of 10 (080)

Clothing 27 of 27 (10) Tool 19 of 23 (083)

Fruit 12 of 12 (10) Vegetable 12 of 12 (10)

Furniture 15 of 15 (10) Vehicle 13 of 14 (093)

Other 53 of 61 (087)

Caramazza and Shelton 11

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

semantic category in this set of items must be inter-preted with caution because the items in each of thecategories are not controlled for potential nuisance vari-ables (ie familiarity frequency and visual complexity) itis clear from Table 4 that EW is not impaired in namingfruits and vegetables Her performance for fruits andvegetables was perfect (100) and strikingly differentfrom that for animals (34)

EWrsquos Naming Decit Is Not Restricted to VisualStimuli Sound Identication

In order to determine whether EWrsquos naming decitmight not reect a category-specic visual agnosia shewas tested with a sound identication task in which theanimal and nonanimal sounds were matched as well aspossible on difculty level as determined by the perfor-mance of several control subjects (see ldquoMethodsrdquo) EWwas quite poor at identifying animal sounds (8 of 32 =025) as compared to nonanimal sounds (20 of 32 =063) a difference that was signicant (z = 306 p lt005) These results suggest that EW does poorly innaming animals across modalities (ie the decit is notrestricted to identifying and naming animals from pic-tures)

Summary

The results we have reported in this section show thatEW has a semantic category-specic naming decit Thedecit is restricted to the category of animals and not tothe category of living things as shown by the fact thatnaming of fruits and vegetables was virtually intactEWrsquos poor naming performance for animals cannot bemerely ascribed to nuisance variables such as familiarityand visual complexity since her disproportionate dif-culties with animals persisted when these variables werestrictly controlled And nally EWrsquos naming decit doesnot appear to be merely the result of a category-specicvisual agnosia because she also showed disproportion-ately poor performance for animals in a sound identica-tion task

Does EW Have a Category-Specic ObjectRecognition Decit

Sartori and Job (1988 see also De Renzi amp Lucchelli1994) reported that their subject Michelangelo whoshowed a category-specic decit for living things wasunable to distinguish between real and unreal animalsand to decide which of four disembodied parts of ananimal went with a body with a missing part This typeof performance has been interpreted as indicating aselective decit for the visual properties of objects How-ever not all cases of category-specic decit are im-paired in object decision tasks There are several reports

of subjects with category-specic decits for livingthings who perform within normal limits in object deci-sion tasks (eg Laiacona et al 1997 Sheridan amp Hum-phreys 1993) Thus impairment in visual object decisionperformance is not a necessary feature of category-specic decit for living things It remains to be deter-mined what implications follow from the associationdis-sociation of impairments at the level of objectidentication and naming We will return to this issue inthe ldquoDiscussionrdquo Here we document that EW has asevere category-specic decit in recognizing animals

Object Decision Task

In this task EW and two control subjects were asked todetermine whether or not each picture represented areal objectmdasheither an animal or some type of artifact(see Figure 1) Performance for all subjects is summa-rized in Table 5 Normal control subjects performed fairlywell on this task EW had signicant problems determin-ing which pictures represented real animals (and therewas a slight tendency to respond Yes in this task) Spe-cically she was barely above chance level (60 correct)in distinguishing between real and unreal animals Shealso had a few difculties distinguishing between realand unreal artifacts (ie was willing to accept someunreal objects as real) but this is a problem shared bythe control subjects and probably reects the difcultyof the ldquounrealrdquo inanimate objects The important point isthat EW performs poorly and well outside the normalrange differentiating real and unreal animals but per-forms within normal range differentiating real and unrealobjects21

Part Decision Task

In this task EW and two control subjects were asked todecide which of two ldquoheadsrdquo went with a headless body(see Figure 2) EW was severely impaired at selectingthe correct head for animals but not for artifacts (60vs 97 z = 345 p lt 005) and her performance with

Table 5 Object Decision Task (Hit = Real)

Subject Hit Correct rejection

EW

Animals 21 of 30 (070) 15 of 30 (050)

Nonanimals 30 of 30 (10) 25 of 30 (083)

Controls

Animals 29 of 30 (097) 25 of 30 (083)

Nonanimals 285 of 30 (095) 22 of 30 (073)

12 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

animals is not signicantly different than chance (z lt 1)Normal controls had no difculty with either category(100 and 97 correct for animals and artifacts respec-tively)

Summary

The results of the Object and Part Decision Tasks areclear EW is severely impaired in discriminating betweenreal and unreal animals but not between real and unrealartifacts She is at chance in recognizing animals but herperformance with artifacts was indistinguishable fromthat of control subjects This pattern of performancerules out the hypothesis that the locus of EWrsquos cate-gory-specic decit is at the stage of name retrieval

EWrsquos Category-Specic Object RecognitionDecit Is Not the Result of Impaired VisualProcessing of Complex Objects

The conclusion reached in the previous section regard-ing the locus of functional decit in EWrsquos category-specic impairment may be challenged It could be ar-gued that the putative category-specic object recogni-tion impairment for animals is merely the result of ageneralized visual recognition decit On this view thereason that EW shows a category-specic decit foranimals is because this category is perceptually morecomplex in the sense that its members are more similarto one another than the members of other categories(eg Gaffan amp Heywood 1993 Humphreys amp Riddoch1987) In order to rule out the possibility that EWrsquosdifculties in visually recognizing animals was the resultof a general visual processing decit we tested herability to perform difcult visual perceptual tasks

Difcult Visual Matching and Categorization TasksThe BORB

EW was administered those sections of the BirminghamObject Recognition Battery (BORB Riddoch amp Hum-phreys 1993) that allow an assessment of her ability toperform complex visual matching and categorizationtasks (see ldquoMethodsrdquo) The tests (Tests 7 8 11 and 12)were administered in the standardized manner She per-formed quite well and within normal range on all tasks

Tests 7 (Minimal Feature Test) and 8 (ForeshortenedView Test) of the BORB are complex visual processingtasks that involve matching a picture of an object seenfrom a ldquostandardrdquo viewpoint to the same object viewedfrom a different nonstandard viewpoint EW performedthese tasks quite well She scored 88 and 84 cor-rectmdashwell within normal limits And she performedawlessly in a similar task (Test 11 Object Matching Test)that required her to match an object (or a part of anobject) to a different view of that object and very well

(93 correct) in an association matching task that re-quires the semantic interpretation of pictured objects

Face Recognition

EW was asked to name pictures of famous people usingthe Boston Famous Faces Task (Albert Butters amp Levin1979) She was given unlimited time to respond Acrossall the faces (across all decades and level of difculty)she performed very well (30 of 56 correct) and withinnormal range for her age group This result suggests thatEW does not have a specic problem processing com-plex visual material such as faces

Summary

There are no indications in the results of our tests ofEWrsquos visual processing performance that she has anyimpairment in visual recognition or categorization otherthan specically for animals These results invite theinference that EWrsquos impairment in visually recognizinganimals is categorically based and most likely has thesame cause as her naming decit

EWrsquos Category-Specic Decit for Animals isNot Modality-Specic

To this point we have documented that EW has a selec-tive decit in naming and recognizing animals and wehave shown that the recognition impairment is unlikelyto merely reect a generalized visual processing defectHere we provide direct evidence that her category-specic decit has a conceptual basis because she isalso impaired in verifying whether an animal has a par-ticular property or attribute (eg Does a giraffe havefour legs) We also address directly the issue of whetherEW has more severe difculty in processing the visualperceptual as opposed to functionalencyclopedic prop-erties of animals As noted in the ldquoIntroductionrdquo thelatter issue is crucial for distinguishing between the SFTand amodal theories of semantic representation

Attribute Processing Task 1 Central Attributes

In this task EW and control subjects were asked todecide whether an attribute statement about an objectis true or false In this and the following attribute tasksonly a subset of the total data was used so that itemscould be matched on familiarity (see ldquoMethodsrdquo sectionfor a description of the matching procedure) The pat-terns of performance on the total data set did not differfrom the patterns reported here Results for EW andcontrol subjects (n = 5) are presented in Table 6 EWhas severe difculties making judgments about animals(z = 539 p lt 005) independent of whether the state-ment involves perceptual or associativefunctional infor-

Caramazza and Shelton 13

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

mation (z lt 05) Thus she only responded correctly to65 of the visual and the functionalassociative attributestatements about animals By contrast her performanceon inanimate objects was very good and fell withinnormal limits

Attribute Processing Task 2 FoodNonfoodAnimals

This task was designed to examine EWrsquos knowledge ofanimals that can be eaten (food animals eg chicken

pig cow) and those that are not typically eaten (bypeople of her generation and cultural background) in theUnites States (nonfood animals eg dog horse robin)The rationale was to examine her visualperceptual andassociativefunctional knowledge of animals that mightbe more familiar to her (food animals) even though theanimals in the ldquofoodrdquo group were matched to the animalsin the ldquononfoodrdquo group on familiarity

As shown in Table 7 EW had severe problems answer-ing questions about animals both for visualperceptualand associativefunctional information and for food andnonfood animals (all zrsquos lt 1) She performed perfectlyhowever when answering the question concerningwhether or not the animal is a food animal (the questionabout edibility was judged to be very easy by controlsubjects)

Attribute Processing Task 3 GeneralSpecic PropertyJudgments

Some properties of a category are shared by all or mostmembers of a category others are specic to one or onlya few members of the category Those properties that aretrue of all members of the category may be more impor-tant or even essential for the inclusion of an object in acategory but they do not contribute to distinguishingamong members of the category Thus for exampleknowing that something has a mouth and eyes may besufcient to classify it as an animal but will not help indeciding whether it is a canary or an eagle By contrastthe information that an object is about the size of achildrsquos st and yellow may be insufcient to supporta decision about whether or not it is an animal butprovides sufcient information for distinguishing be-tween an eagle or a canary We will refer to the formerknowledge as general-attribute and the latter as specic-attribute knowledge22 An important question concernsthe level of knowledge that is damaged in EW Is sheequally impaired with general- and specic-attributeknowledge

The motivation for this question springs in part from

Table 6 Central Attributes Judgment Task (proportioncorrect range for control subjects)

EW Animals Objects

Visualperceptual

True 38 of 59 (064) 54 of 59 (092)

False 26 of 39 (067) 37 of 39 (095)

Associativefunctional

True 20 of 30 (067) 30 of 30 (10)

False 17 of 27 (063) 26 of 27 (096)

Controls Animals Objects

Visualperceptual

True 092ndash098 092ndash10

False 085ndash10 086ndash10

Associativefunctional

True 093ndash10 093ndash097

False 096ndash10 092ndash10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) visualperceptual rating for true state-ments is 485 (022) and for false statements is 475 (031) Themean associativefunctional rating for true statements is 492 (024)and for false statements is 488 (015)

Table 7 FoodNonfood Animal Attributes Judgment Task (proportion correct range for control subjects)

Subject Food Animal Nonfood Animal

EW

Visualperceptual 27 of 41 (066) 26 of 41 (063)

Associativefunctional 32 of 41 (078) 32 of 41 (078)

Controls

Visualperceptual correct 083ndash093 085ndash10

Associativefunctional correct 088ndash093 081ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 469 (038) The mean asso-ciativefunctional rating is 472 (038)

14 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

the observation that EW is quite capable of distinguish-ing animals from artifacts (though she cannot distinguishbetween real and unreal but possible animals) Thisraises the issue of whether her ability to categorize anobject as ldquoanimalrdquo also allows her to access general-attribute knowledge about animals In the eventualitythat she could systematically access such information itwould establish that she is not confused about what ananimal is but only about detailed distinctions amongcategory members To test this possibility EW and con-trol subjects (n = 2) were asked to decide whethergeneral- and specic-attribute knowledge statementsabout an object are true or false (see ldquoMethodsrdquo fordetails) The results are shown in Table 8 and clearlydemonstrate that EW has no difculty with questionsconcerning attributes that are shared by all (or almostall) members of a category Because of this controlsubjects did not complete these questions EW per-formed almost perfectly with specic-attribute informa-tion about inanimate objects (and better than bothcontrol subjects) and much worse with specic-attributeinformation for animate objects (z = 469 p lt 005)Similar to the pattern of performance on the previousattribute judgment tasks her knowledge of specic at-tributes of animals is equally disrupted for visual and forassociativefunctional information (z lt 1)

Attribute Processing Tasks Collapsing Across Tasks

The pattern of performance across the attribute judg-ment tasks reported thus far is clear EW has severe

problems with the attributes of animate objects regard-less of whether or not they relate to visual properties orto associative properties and has no problem with attrib-utes of inanimate objects For animals the only questionson which she performs very well are general-attributeknowledge questions indicating that she knows thatanimals have eyes and mouths and that they breathe anddigest food but little else besides that

To examine further her performance with visualper-ceptual and associativefunctional information for ani-mals and nonanimals we collapsed her data across allthe attribute judgment tasks This gives us a very largenumber of data points in each cell as well as a range ofdifculty of questions Performance is summarized inTable 9 for matched items Although there is a smalladvantage for associativefunctional information over vis-ualperceptual information for animals this difference isfar from signicant (z = 07974 p gt 005) and is onlyslightly larger than a similar difference for inanimateobjects

Attribute Processing Task 4 Shared Attributes

Although the evidence presented thus far on attributejudgments would seem to indicate that EW has a cate-gory-specic decit for animals there remains the possi-bility that the putative modality-specic nature of thedecit merely reects a selective decit in processingcertain attributes that happen to be differentially distrib-uted across semantic categories That is there is thepossibility that the problem concerns the properties

Table 8 GeneralSpecic Attributes Judgment Task (proportion correct range for control subjects)

General Specic

Subject Visual Associative Visual Associative

EW

Animals 130 of 130 (10) 129 of 130 (099) 74 of 100 (074) 115 of 150 (077)

Inanimate 60 of 60 (10) 75 of 75 (10) 100 of 100 (10) 149 of 150 (099)

Controls

Animals ndash ndash 092ndash094 085ndash098

Inanimate ndash ndash 087ndash093 082ndash088

Note On the rating scale 1 = just guessing and 5 = extreme condence The mean (SD) visualperceptual rating is 491 (023) The mean asso-ciativefunctional rating is 486 (023)

Table 9 Matched Data Collapsed Across All Attribute Judgment Tasks (proportion correct)

Animals Inanimate objects

Visualperceptual 202 of 301 (067) 217 of 226 (096)

Associativefunctional 223 of 300 (074) 217 of 219 (099)

Caramazza and Shelton 15

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

themselves and not the semantic category of animals Ifthat were the case a category-specic decit emergedonly because we queried different properties for animalsand nonanimals and these properties just happened tobe differentially damaged To circumvent this potentialproblem EW was tested in two attribute judgmenttasks with the same attributes for animate and inanimateobjects23

Attribute Processing Task 4a Size Judgments In thistask EW was asked to decide which of two animate ortwo inanimate objects is the larger of the two Perfor-mance is summarized in Table 10 and demonstrates thatEW had more difculty with animal size judgments thaninanimate size judgments (z = 183 p lt 006) and isoutside the normal range for the animal category but notthe inanimate category

Attribute Processing Task 4b Other Shared AttributesIn this task EW was asked to decide whether a propertystatement about animate and inanimate objects was trueor false (see ldquoMethodsrdquo for examples of the propertiesincluded in the task) Performance is summarized in Table10 and indicates that EW had much more difculty withattributes of animate items than those same attributesassociated with inanimate items (z = 338 p lt 005)

Attribute Processing Task 5 Visible and Not VisibleAttributes

EWrsquos performance in the preceding two tasks showsthat her decit involves the category of animate objectsand is not specic to attribute concepts found exclu-sively with animals As a further test of her ability toprocess the attribute concepts that she is unable toverify in the context of judgments about animals weasked her to answer questions about properties of pic-tured animals in one of two conditions when the prop-

erties were visible and when they were not visible in thepictured animal Thus for example EW was asked todecide whether a horse has a tail when shown a pictureof a horse with a tail and when shown a picture of ahorse from a perspective that did not show its tail Thecrucial issue is whether she can answer attribute ques-tions correctly when the information is available in thepictured object but answers incorrectly when the infor-mation is not given in the picture EW had no problems(100 correct) answering the attribute questions whenthe information was available in the picture but hadserious problems (55 correct) when the informationwas unavailable in the picture (z = 728 p lt 005)

Summary

The results of the attribute processing tasks show thatEWrsquos category-specic decit extends beyond her nam-ing and picture recognition difculties to involve lan-guage comprehension Her decit appears to beconceptually based and is not just a decit of visualperception or of lexical access in production The resultsalso clearly show that EWrsquos decit involves equally thevisualperceptual and the functionalassociative proper-ties of animate objects And nally her difculties withobject attributes are the result of a category-specicimpairment for animate objects and not a generalizeddecit for those attribute concepts In short the resultsshow that EW has a semantic category-specic decit

DISCUSSION

The results we have reported can be summarized asfollows

1 EW has a category-specic decit restricted to thecategory of animate objects She is disproportionatelyimpaired in naming animals relative to other living thingssuch as fruits and vegetables and relative to all otherinanimate categories tested including food items Thecategory-specic nature of the decit persisted understrict control of potential nuisance factors such as itemfamiliarity visual complexity frequency or their combi-nation

2 EW has a category-specic decit in visually (andauditorily) recognizing animate objects She is dispropor-tionately impaired in recognizing animals relative toother living items and artifacts This decit is not theresult of a generalized perceptual processing decit in-teracting with differential levels of visual complexityacross categories EW performed within normal limits incomplex visual processing tasks

3 EW has a category-specic decit in language com-prehension In various types of attribute processing tasksshe performed very poorly with statements about ani-mate objects but performed within normal limits withstatements about other living things and artifacts This

Table 10 Size Judgments Task and Matched AttributesJudgments Task (proportion correct range for controlsubjects)

Size Judgments

Subject Animals Inanimate

EW 13 of 18 (072) 17 of 18 (094)

Controls 094ndash10 094ndash10

Matched Attributes Judgments

Subject Animals Inanimate

EW 32 of 42 (076) 42 of 42 (10)

Controls 094ndash097 10

Note On the rating scale 1 = just guessing and 5 = extremecondence The mean (SD) rating is 497 (009)

16 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

selective decit persisted in the face of stringent controlsof various nuisance variables

4 EWrsquos category-specic decit for animals is notalso modality-specic (for visual knowledge) In variousattribute processing tasks she consistently performedequally poorly with visual and functionalassociativestatements of animate objects and equally well andwithin normal limits for all attributes of inanimate ob-jects

The facts 1 through 4 allow several conclusions aboutthe nature of EWrsquos decit EWrsquos selective impairmentin recognizing and naming animate objects is not re-stricted to the recognition of visually presented stimulibut extends to auditory stimuli as well and the fact thather impairment extends to language comprehensiontasks (facts 1 through 3) allows the inference that herdecit involves the semantic system and not simply thevisual recognition or the word production systems Fact4mdashEWrsquos selective impairment concerning animate ob-jects is equally severe for their functionalassociative andvisual attributesmdashallows the inference that the damagedsystem is not organized by ldquomodalityrdquo that is the dam-aged system does not represent visual and functionalassociative knowledge in distinct subsystems

These conclusions have important implications for theissues raised in the ldquoIntroductionrdquo concerning the organi-zation of conceptual knowledge in the brain First theyare at variance with the sensoryfunctional theory (SFT)of semantic category-specic decits (Farah amp McClel-land 1991 Silveri amp Gainotti 1988 Warrington amp Shal-lice 1984) and thus provide a clear refutation of thistheory of semantic organization Second they are consis-tent with the hypothesis of amodal organization of thesemantic system as proposed by the organized unitarycontent hypothesis (OUCH Caramazza et al 1990) Andthird they encourage the hypothesis of domain-specicorganization of knowledge in the brain We discuss eachof these issues in turn

Refutation of the SensoryFunctional Theory ofCategory-Specic Decits

The SFT makes two clear predictions concerning cate-gory-specic decits One prediction is that category-specic decits should not honor ldquonarrowrdquo semanticcategory boundaries but should instead be determinedby the role played by visual (sensory) features in deter-mining the meaning of category members This translatesinto the expectation that the categories of animals andfruits and vegetables (as well as other visually weightedcategories) should be damaged together The other majorprediction is that category-specic decits for livingthings should necessarily also be modality-specic in thesense that knowledge of visual properties must be dis-proportionately impaired relative to knowledge of func-tionalassociative properties Neither prediction held up

in our investigation of EW Her category-specic decitis restricted to the category of animals leaving unaf-fected her knowledge of fruits vegetables and artifactsand her knowledge of functional associative attributesof animals is as impaired as her knowledge of their visualattributes

Other results in the literature are highly problematicfor the SFT The case of selective sparing of the categoryof animals (Hillis amp Caramazza 1991) and of subjectswith selective damage of the category of fruits andvegetables (Farah amp Wallace 1992 Hart et al 1985)complement the results reported for EW (which showthat she has a selective decit for animals) These resultsjointly establish that category-specic decits can bevery narrow involving separately the categories of ani-mate objects and the category of fruits and vegetablesthus undermining the expectation derived from the SFTthat the categories of living things should be damagedtogether The other set of results that converges withEWrsquos performance in undermining the SFT concernsreports of subjects with category-specic decits forliving things who do not show a disproportionate decitfor visual attributes of living things (Funnell amp DeMornay Davies 1997 Laiacona Barbarotto amp Capitani1993 Laiacona et al in press Sheridan amp Humphreys1993) Thus on this issue too there is no support for theSFT

There remain two other sources of evidence that havebeen cited in support of the SFTmdashthe results of someneuroimaging studies (eg Martin Wiggs Ungerleider ampHaxby 1996) and the results of computational modeling(Farah amp McClelland 1991) We will discuss the neuro-imaging results in greater detail in a later section Hereit sufces to say that some of the neuroimaging resultsare consistent with the SFT but they are also consistentwith alternative interpretations Thus these results donot help distinguish between alternative theories of se-mantic organization We begin with a discussion of theputative evidence from computational modeling

Farah and McClelland (1991) purport to show thatdamage to the visual component of a modality-organizedsemantic system can explain the existence of category-specic decits They did this by developing a paralleldistributed processing (PDP) model in which semanticknowledge is subdivided into visual and functional com-ponents The two major assumptions of this model arethat visual and functional semantic properties are repre-sented in separate but interconnected networks and thatthe ratio of visual to functional properties for livingthings is much larger than that for nonliving thingsWhen the visual components of various networks imple-menting these assumptions were lesioned the resultingpatterns of performance mimicked the category-specicdecit for living things and the reverse dissociation wasobtained when the functional component of the net-work was lesioned This pattern of results provides anexistence proof that a category-specic decit can be

Caramazza and Shelton 17

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

obtained without having to postulate categorical organi-zation of semantic knowledge

As an existence proof that category-like effects canemerge from a noncategorically organized semantic sys-tem the results reported by Farah and McClelland (1991)need not be controversial nor even surprising for thatmatter In some respects the results of the implementedmodel merely reect their assumption that the meaningof living things is much more dependent on visual prop-erties than is the case for nonliving things24 In theirmodeling experiments the ratio of visual to functionalproperties for living things was set to 16121 and fornonliving things it was set to 9467 Thus damage tothe visual semantic network could hardly result in any-thing but more severe difculty for living than nonlivingthings Put differently the highly disproportionate ratiosof visual to functional properties for the categories ofliving and nonliving things can be seen as roughly ap-proximating a categorical distinction between the twosemantic domains The model merely capitalizes on thiscorrelation As noted by Farah and McClelland (1991)ldquoThe ability of a modality-specic semantic memory ar-chitecture to account for category-specic semanticmemory impairments depends of course on there beinga correlation between modality of knowledge and cate-gory of knowledgerdquo (p 355) If there were no suchcorrelation it would not be possible to devise a modal-ity-based explanation for category- specic decits Thusthe ultimate value of the modeling demonstration de-pends entirely on the validity of the empirical assump-tions made by the model that is the assumptions aboutthe ratios of visual to functional properties for the livingand nonliving categories respectively

Warrington and her collaborators (Warrington ampMcCarthy 1983 1987 Warrington amp Shallice 1984) hadsuggested that living things are known and distinguishedprimarily through their visual attributes whereas nonliv-ing things are known primarily through their func-tionalassociative properties This suggestion was basedon mere intuition however Farah and McClelland (1991)attempted to provide an empirical foundation for thisintuition They did this by counting the number of visualand functional descriptors that subjects identied indictionary denitions of the living and nonliving thingsused by Warrington and Shallice (1984 Experiment 2)They found that subjects underlined more visual descrip-tors for living than nonliving things (an average of 268and 157 respectively) but many fewer functional de-scriptors for living than nonliving things (an average of035 and 111 respectively) Thus the ratio of visual tofunctional properties was found to be far higher forliving (771) than nonliving things (141) These resultsseem to conrm the speculation about the relative im-portance of visual and functional-associative propertiesin determining the meaning of living and nonlivingthings However there is a serious aw in the experimen-tal procedure used by Farah and McClelland that makes

interpretation of their results problematic at best Theproblem concerns the instructions given to subjects onwhat to count as visual and functional-associative de-scriptors

Farah and McClelland (1991) asked their subjects tounderline either visual or functional descriptors indenitions of living and nonliving things Subjects in thevisual descriptor condition were asked to underline allwords referring to the visual appearance of an itemSubjects in the functional descriptor condition wereasked to underline ldquoall occurrences of words describingwhat the item does or what it is forrdquo (p 342 emphasisadded) Now it is clear that all objects living and nonliv-ing can be described by reference to their visual appear-ance and therefore counting the visual descriptors indenitions of items in the two categories may provide afair estimate of the sensory properties known by sub-jects about various objects However asking subjects tounderline ldquowhat it is forrdquo for living and nonliving thingswill not provide a fair estimate of the nonsensory prop-erties known for living things That is because the useof an itemmdashwhat it is formdashis a highly specic propertytypically found with artifacts but not natural kinds hav-ing a ldquofunctionrdquo is almost a distinguishing feature be-tween living things and artifacts It is meaningful to askldquoWhat is a table or a knife forrdquo but barely felicitous toask ldquoWhat is a lion or a squirrel forrdquo Thus it is hardlysurprising that Farah and McClelland found large discrep-ancies in the ratios of visual to functional descriptors forliving and nonliving categories these discrepancies areentirely due to the instructions given to subjects onwhat could count as a functionalassociative feature Wecan easily imagine reversing the ratios of visual to func-tional properties for living and nonliving things by in-structing subjects to underline visual properties that arefound almost exclusively in nonliving things such as ldquohaswheel-like featuresrdquo ldquohas straight edgesrdquo ldquohas wood-liketexturerdquo and so on In this case we would most likelynd that nonliving things would have a larger ratio ofvisual to functionalassociative attributes than livingthings

It is crucial that the criteria for identifying the sensoryand nonsensory properties of living and nonliving thingsnot contain a built-in category bias However the instruc-tions Farah and McClelland (1991) gave their subjectseffectively led them to exclude from consideration suchimportant nonsensory properties of living things as ldquolivesin desertrdquo ldquoferociousrdquo ldquocarnivorerdquo ldquoherbivorerdquo ldquodomesti-catedrdquo ldquosolitaryrdquo ldquoediblerdquo ldquoegg-layingrdquo and so on If theseand other nonsensory properties had not been excludedby the instructions biasing subjects to consider onlyldquowhat it is forrdquomdashprincipally a property of artifactsmdashthedifferences in the ratios of sensory to nonsensory prop-erties for living and nonliving things would not havebeen nearly as large as reported by Farah and McClel-land Indeed when we instructed two groups of subjectsto underline either all sensory properties or all non-

18 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

sensory properties in the denitions of the living andnonliving items used by Farah and McClelland25 weobtained the following ratios of sensory to nonsensoryproperties for living and nonliving things 2925 and2223 respectively26 Similar results have recently beenobtained by McRae de Sa and Seidenberg (1997) usinga different procedure to estimate the ratio of visual tofunctional attributes for living and nonliving categoriesThese ratios do not provide empirical support for theassumption that there is a correlation between ldquomodalityof knowledge and category of knowledgerdquo27

In this section we have argued that neither of themajor expectations derived from the SFTmdashthe predictedcorrelation of category decits and the predicted co-occurrence of category- and modality-specic decitsmdashreceives support from EWrsquos performance or theperformance of other reported cases of category-specicdecit We have also argued that the computational mod-eling evidence (Farah amp McClelland 1991) offers nomore than an existence proof that category-like effectscan result from damage to noncategorically organizedsubsystems whose contents are correlated with seman-tic categories However the success of the computa-tional modeling demonstration does not require that thecontents of the subsystems be modality-specic All thatit requires is that there be a correlation between thecontents of specic subsystems and semantic categoriesThe contents of subsystems can vary from completelynonoverlapping (categorical) representations to modal-ity-specic subsystems that are correlated with differentsemantic categories (SFT) to modality-neutral clumps ofintercorrelated semantic properties that are correlatedwith different semantic categories (OUCH) Thus thecomputational modeling demonstration reported byFarah and McClelland would only be useful in distin-guishing between the SFT and alternative accounts ofcategory-specic decits if its assumptions about thecontents of the hypothesized subsystems could be mo-tivated empirically However we have argued that theempirical evidence provided by Farah and McClellandfor a putatively large discrepancy in the ratios of visualto functionalassociative properties for living and nonliv-ing things is tainted by having inappropriately restrictedwhat could count as a functionalassociative attribute(because only ldquowhat is it forrdquo attributes were allowedfavoring the kinds of attributes that artifacts but notanimals are likely to have) And we have gone on toshow that the ratios of visual to functionalassociativeproperties for living and nonliving things are in factapproximately equal when subjects are instructed tocount all perceptual and all nonperceptual (func-tionalassociative) descriptors Thus the central assump-tions about the nature of the semantic subsystems in themodel proposed by Farah and McClelland are withoutempirical foundation thereby undermining the value ofthe computational modeling demonstration as evidencein support of the SFT

The Organized Unitary Content HypothesisRevisited

The organized unitary content hypothesis (OUCH)makes two clear predictions Category-specic decitscan be narrower than the livingnonliving distinctionand category-specic decits are not also modality-specic EWrsquos performance is in agreement with bothpredictions from the OUCH (1) Her decit is restrictedto the category of animate things and (2) she is equallyimpaired in processing the visual and functionalassocia-tive attributes of animals and of no other semantic cate-gory The modelrsquos major drawback is that OUCH does notprovide a principled explanation for the attested pat-terns of category-specic decits It fails to explain whythe unambiguous cases of category-specic decit seemto respect the tripartite distinction animalplantartifact(and not some other pattern of category-specic de-citsmdashie why not a selective decit for aquatic animals)and why the most prevalent category-specic decitinvolves the category of animals Thus although OUCHmay provide a useful noncategorical framework withinwhich to explore various aspects of semantic memorydecits including their category-specic form we mayhave to consider a radically different theoretical frame-work to explain the high prevalence of selective de-cits for animals and the tripartite distinction animalplantartifact in the occurrence of category-specicdecits

Domain-Specic Organization of ConceptualKnowledge in the Brain EvolutionaryAdaptations

None of the evidence reviewed here including EWrsquosperformance compels us to adopt the view that concep-tual knowledge is organized categorically in the brainHowever doing so provides a natural explanation forprecisely that feature of the phenomenon of category-specic decits that has proven to be most problematicfor the reductionist accounts the fact that the categoriesof animals fruits and vegetables and artifacts can bedamaged independently of each other On this view theempirically observed tripartite distinction of category-specic decits follows directly from the assumptionthat these and only these three categories form the basisfor the organization of conceptual knowledge But theexplanatory power of this assumption would amount tonaught unless it could be given independent theoreticaland empirical justication That is unless we can inde-pendently motivate the assumption of categorical organi-zation of conceptual knowledge we would have merelyassumed what we are trying to explainmdashan infelicitouscircularity It is important therefore to determinewhether there might not be theoretical arguments andempirical evidence that could be used to independently

Caramazza and Shelton 19

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

support the assumption that conceptual knowledge isorganized categorically

In the ldquoIntroductionrdquo we speculated that adoption ofan evolutionary perspective to the problem of how con-ceptual knowledge is organized in the brain might pro-vide the motivation for assuming that it is organizedcategorically It is not implausible to assume that evolu-tionary pressures led to specic adaptations for recog-nizing and responding to animal and plant life (the latteroperationally represented by fruits and vegetables inresearch on category-specic decits) The tness valuefor these adaptations are obvious Animals are potentialpredators but also a potential source of food plants area source of food and medicine The ability to recognizeand respond quickly to types of animals has clear sur-vival and reproductive value as does the ability to accu-rately distinguish among different plants for theiralimentary and medicinal value In perceptual and cog-nitive terms these adaptations might consist of special-ized processes for the rapid and accurate classicationof objects as animals as plant life or as neither of thesetwo categories of objects In terms of neural mecha-nisms the relevant adaptations might consist of dedi-cated neural circuits for processing animals and plantlife And because of the clear affectiveemotional compo-nent associated with ight and feeding responses toanimals and plant life it is not implausible to furtherassume that the neural adaptations would involve cir-cuits that include the limbic system If these speculationswere to be even approximately correct we would havethe independent motivation we have been seeking insupport of the assumption that conceptual knowledge isorganized categorically in the brain The evolutionaryadaptations for recognizing animals and plant life wouldprovide the skeletal neural structures around which toorganize the rich perceptual conceptual and linguisticknowledge modern humans have of these categories

An important implication that follows from the adop-tion of an evolutionary perspective on the organizationof conceptual knowledge in the brain is a restriction onwhat is likely to count as evolutionarily signicant se-mantic categoriesmdashthat is categories for which it isplausible to propose that their successful recognitionwould have tness value We have argued that animalsand plant life satisfy the latter criterion Whether or notthe ability to recognize and use ldquotoolsrdquo should also beaccorded tness value is less obvious although not im-plausible (see Hauser in press) However it is not neces-sary that tools be accorded such status for the argumentdeveloped here It is sufcient that the categories ofanimals and plant life be distinguished from ldquootherrdquo cate-gories Thus on this view the only ldquotruerdquo category-specic decits28 will be those involving the categoriesof animals plant life and (by contrast) artifacts and notother ner-grained distinctions such as land animalsfruits kitchen utensils and so on

Another implication that follows from the assumption

that evolutionary adaptations provide the basis for thecategorical organization of conceptual knowledge in thebrain is that the incidence of category-specic decitsfor living things should be greater than that for nonlivingthings This implication is derived from the suppositionthat specialized neural mechanisms are more likely to behighly localized and consequently more prone to selec-tive damage This expectation would seem to have somesupport Most category-specic decits that have beenreported over the past 15 years have involved the cate-gories of living things Of course it could be that someof the putative category-specic decits for living cate-gories are merely artifacts of inadequate stimulus con-trols (Stewart et al 1992 Funnell amp Sheridan 1992)However as discussed extensively in the ldquoIntroductionrdquothere is now a substantial number of well-studied casesof category-specic decits for living categories that can-not be dismissed as methodological artifacts (see forexample cases in Laiacona Barbarotto amp Capitani 1993Laiacona et al 1997) Thus even with a major correctionfor possible methodological artifacts in the early studiesof category-specic decits the discrepancy betweenthe incidence of selective impairment for the living andnonliving categories remains striking

A further implication of the view that there might bededicated neural circuits for the categories of animalsand plant life involves the category of foods Because theassumed neural circuitry for animals and plant life in-volves the limbic system it is not unreasonable to sup-pose that the semantic category of foods might sharesome of its neural circuitry Consequently damage toneural structures that affect the categories of animals orof fruits and vegetables are also likely (though not nec-essarily) to result in impairment of the category of foodseven though many members of the latter category aremore properly considered artifacts (consider for exam-ple spaghetti fudge hamburger and so on) This assump-tion would explain why some cases of category-specicdecits for living categories also show impairments forfoods

The hypothesis that knowledge is organized categori-cally in the brain provides a good account of extantresults on semantic category-specic decits Howeverit is important to stress here that the appeal to evolu-tionary pressures as a possible causal basis for the cate-gorical organization of knowledge in the brain is notnecessarily incompatible with the cognitive principlesthat characterize the OUCH and SFT proposals Indeedit is quite likely that both domain-specic and domain-general learning principles are involved in the organiza-tion of conceptual and linguistic knowledge in the brainThe domain-specic principles have a very narrow rangeof applicability and serve only to explain why it mightbe the case that knowledge of animals and of plant lifeis represented in distinct neural circuits This account issilent on the larger issue of how conceptual knowledgewithin the broad categories of living and nonliving

20 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

things is organized And it could very well turn out thatdomain-general principles such as those invoked underOUCH (or SFT although no empirical support has beenfound for this account) provide the basis for the organi-zation of conceptual knowledge within the distinct cate-gories of animals plant life and artifacts

Domain-Specic Organization of ConceptualKnowledge in the Brain OntogeneticConsiderations

The idea that neural adaptations are responsible for theorganization of conceptual knowledge in the brain hasdirect implications for theories of acquisition of thisknowledge Specically this thesis implies that thereshould be specialized mechanisms for the recognitionand categorization of the members of the categories forwhich specic adaptations have evolved And in fact thecontrasting viewpoints about the possible bases for theexistence of semantic category-specic decits havetheir counterparts in the developmental literature Therethe issue has been framed in terms of whether cognitivedevelopment is to be understood as the product ofdomain-general or domain-specic processes The do-main-general view holds that a common set of verypowerful learning mechanisms underlies the acquisitionof all forms of knowledge from mathematical to musicalskills and from language to the ability to play backgam-mon This position is most clearly represented by theclassical empiricist theories of learning and memory(eg Skinner 1957) and more recently by connectionisttheories (eg McClelland amp Rumelhart 1986) The do-main-specic view holds that highly specialized dedi-cated mechanisms are involved in the acquisition ofspecic types of knowledge (Carey 1985 Pinker ampBloom 1990 Sperber 1994) The best-known domain-specic theory is the theory of universal grammar oflanguage acquisition proposed by Chomsky (19801986) However domain-specic theories have also beenproposed for speech perception (Liberman amp Mattingly1989) naive physics and psychology (Carey amp Spelke1994) number (Carey amp Spelke 1994 R Gelman 1990)the animate-inanimate distinction (R Gelman 1990) folkbiology (Atran 1995 Sperber 1994) and more generallyvarious aspects of animal learning (Rozin amp Schull 1988)In each case it could be proposed that specialized cog-nitive mechanisms reecting adaptations in response toevolutionary pressures are responsible for the acquisi-tion of a specic type of knowledge (for recent reviewssee papers in Hirschfeld amp S Gelman 1994 SperberPremack amp Premack 1995)

Of particular relevance here is the proposal that theacquisition of the animate-inanimate distinction involvesdomain-specic mechanisms Although alternative pro-posals have been offered concerning the precise natureof the content of the domain-specic mechanism foracquiring the animate-inanimate distinction (see Atran

1995 Carey 1985 1995 R Gelman 1990 R Gelman ampBrenneman 1994 R Gelman Durgin amp Kaufman 1995Keil 1994 Sperber 1994) they all maintain that a set ofinnate principles guides its acquisition These principlesdo their work by specifying the core content of the twocategories Their major function is to direct attention tothe relevant exemplars of the categories by focusing onthe salient distinctions among them Candidate featuresof the environment that could serve the function ofldquotriggeringrdquo a rst-pass distinction between categoriesinclude the motion patterns of objects and their physicalappearance (Mandler 1992) However the perceptualdistinctions are not themselves criteria for distinguishingbetween categories They merely function as cues tocategory membership The categorical distinction is fun-damental and precedes the acquisition of specic per-ceptual facts about their members In other words theperceptual features of objects are powerful cues tosameness of category but they do not constitute thecore properties of the animate-inanimate distinction Thelatter are more likely to be complex properties that donot correspond to any simple perceptual feature Thuscandidate core properties for animate objects might betheir internal structure (eg having organs) whetherthey are capable of self-initiated motion and whethertheir motion patterns can be construed as having inten-tional cause (Premack 1990) for artifacts a core prop-erty might be their intended function (Bloom 1996)

There is considerable evidence in favor of the domain-specic thesis of the acquisition of the animate-inanimate distinction Perhaps the most compelling re-sults are those concerning the infantrsquos ability to distin-guish physical from psychological (biological) causalityRecent experiments have shown that infants as young as3 months understand many aspects of the structure ofthe physical world For example they understand someof the distinguishing properties of the concepts of solid-ity and support and they understand that two objectscannot occupy the same space at the same time (Baillar-geon 1993 Spelke 1988) Furthermore this knowledgeis embedded in a larger conceptual scheme that involvesobject motion and the concept of causality Spelke Phil-lips and Woodward (1995) have identied a set of coreprinciples about the infantrsquos understanding of objectsmdashthe principles of cohesion continuity and contactmdashwhich function to constrain the interpretation of anobjectrsquos motion For example the principle of contactunderlies the infantrsquos understanding that objects canonly act on each other by touching There is a large bodyof evidence that very young infants understand the dis-tinction between caused and uncaused motion throughthe principle of contact Thus 4-month-old infants candistinguish between the implicit causality in a ballrsquosmotion when it is launched by another moving objectand the very similar but fundamentally different casewhere the two objects are separated either by a brieftemporal lag or by a small spatial gap (Leslie 1982 1984

Caramazza and Shelton 21

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

Leslie amp Keeble 1987) These results together with otherrecent evidence that shows that infants suspend appli-cation of the contact principle when reasoning abouthuman (and perhaps animal) actions (Spelke et al 1995)suggest that they are able to distinguish correctly be-tween animate and inanimate objects (for otherwisethey would not know when to apply and when tosuspend the contact principle) More generally it hasbeen supposed that a core property of the infantrsquos con-cept of human (and perhaps animal) is the principle ofldquoself-propelled motionrdquomdasha concept intimately related tothe distinction between mechanical and intentionalagency (see R Gelman 1990 Premack 1990 Mandler1992)

There are two other important sources of evidence insupport of the infantrsquos precocity in distinguishing ani-mate from inanimate objects One is the infantrsquos well-documented ability to distinguish biological fromnonbiological motion Bertenthal and his collaborators(Bertenthal 1993 Bertenthal Proftt amp Cutting 1984)have shown that infants as young as 3 months canreliably distinguish point-light displays of motions pro-duced by animate and inanimate objects The other evi-dence concerns the infantrsquos ability to categorize staticrepresentations of objects (toy gures and pictures)Mandler and her collaborators (Mandler 1992 1994Mandler Bauer amp McDonough 1991 Mandler ampMcDonough 1993) have shown that 9-month-old infantscan distinguish between animals and vehicles evenwhen between-category similarity is controlled Using adishabituation paradigm they have found that infantsdishabituate to airplanes but not dogs cats or rabbitsafter seeing birds even though birds were shown withoutstretched wings and thus were more ldquoperceptuallysimilarrdquo to airplanes than they were to dogs cats orrabbits This pattern of results suggests that infants makea global differentiation between animals and artifactsbefore they fully appreciate the basic-level categorieswithin these conceptual domains (but see Quinn ampEimas 1996 for a different interpretation) Thus the evi-dence from infantsrsquo precocious categorization of animateand inanimate toy objects as well as the evidence fromtheir precocious distinction of point-light displays ofanimate and inanimate motion suggest that the distinc-tion may be subserved by specialized domain-specicmechanisms

In this section we have argued that recent develop-ments in the area of concept acquisition provide impor-tant converging evidence for the proposal thatconceptual knowledge is organized categorically in thebrain The evidence conrms the expectation derivedfrom the claim that evolutionary adaptations form thebasis for the hypothesized categorical organization ofconceptual knowledgemdashnamely that the concepts ofanimal and artifact are acquired through the operationof innate domain-specic mechanisms

Neuroanatomical Considerations

The neuroanatomical basis for semantic category-specic decits has been addressed both throughanatomo-clinical correlations and through functional im-aging of the intact brain The investigation of anatomo-clinical correlations has produced relatively clear thoughnot unequivocal results The picture is clearest for casesof selective decit for living things Most of these caseshave sustained damage to the left temporal lobe (as wellas the right temporal lobe in patients recovering fromherpes simplex encephalitis see Gainotti Silveri Danieleamp Giustolisi 1995 Saffran amp Schwartz 1994 for reviews)However some of the patients with disproportionatedecit for living things have also sustained damage tofrontal and to inferior parietal areas (the case reportedhere Hillis amp Caramazza 1991 Laiacona Barbarotto ampCapitani 1993) or extensive damage due to trauma(Farah et al 1989 Laiacona Barbarotto amp Capitani1993) The pattern of anatomo-clinical correlations is lessclear for cases of selective impairment to the categoryof artifacts Lesions associated with the latter pattern ofdecit have been more variable and have typically in-cluded fronto-parietal areas but also the temporal lobein some cases (for reviews see Gainotti et al 1995Saffran amp Schwartz 1994) A rough generalizationfrom this literature is that the categories of livingthings are associated with temporal and sometimesfrontal and parietal lobe lesions whereas impairmentof the category of artifacts is associated with moredorsal lesions involving temporal parietal and frontalareas

Most cases of category-specic decits have been in-terpreted as involving damage to the semantic systemallowing inferences about the possible organization ofsemantic knowledge in the brain An alternative proposalhas been offered by Damasio et al (1996) who reportedthe most extensive investigation of the neuroanatomicalbasis for category-specic decits to date These investi-gators argued that category-specic naming decits neednot result from damage to the semantic system but canresult from damage to the lexical representations medi-ating between the semantic and the phonological con-tent of words On this view the analysis of patterns ofcategory-specic decits can inform hypotheses aboutthe organization of lexical (as opposed to semantic)knowledge in the brain In their investigation of a largenumber of patients with single focal lesions whoshowed category-specic decits (N = 30) Damasio etal found that impairment for the category of animals isassociated with damage to the left inferotemporal(mostly anterior) area and impairment for tools is asso-ciated with damage to the posterolateral inferotemporalarea and the junction of temporo-occipital-parietal cor-tices Thus despite differences in the functional interpre-tation of category-specic decits29 the results of this

22 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

study further conrm the important role of the lefttemporal lobe in the representation of knowledge aboutthe category of animals and the role of more dorsal areasfor artifacts

The results from functional neuroimaging experi-ments are somewhat unclear Three PET studies havedirectly compared performance for living things andartifacts (Damasio et al 1996 Martin et al 1996 Peraniet al 1995) All three studies show segregation betweencategories but the specic areas involved differ acrossstudies For the living things category Perani et al andMartin et al found activation of the occipital lobes bilat-erally and the inferior temporal lobe (bilaterally by Per-ani et al left only by Martin et al) For the artifactcategory Perani et al found mostly left-sided activationof the lingual parahippocampal gyri middle occipitalgyrus and dorsolateral frontal regions Martin et al foundactivation of the fusiform gyri of the temporal lobesbilaterally and left inferior frontal region and left precen-tral gyrus By contrast Damasio et al (whose study fo-cused on activations of regions of the temporal lobe)found that naming animals resulted in activation of theleft inferotemporal area and naming of tools resulted inactivation of posterior middle and inferior temporal gyriThus there is some agreement among the three studiesThe inferior temporal lobe is activated in processinganimals the posterior middle temporal area may be moreimportant for tools In addition there are indications thatthe frontal lobes may be important not only for tools(Martin et al and Perani et al) but also for animals(Martin et al) Finally animal naming more strongly acti-vates the occipital lobes bilaterally

It is not implausible then to conclude that the lefttemporal lobe is crucially involved in some aspect oflexical-semantic processing as may be parts of the leftfrontal lobe Although Damasio et al (1996) interpret thefunction of the different areas of the left temporal lobeactivated in naming animals and artifacts as involvingmechanisms of lexical retrieval as opposed to semanticknowledge this conclusion is premature at best (seeNote 29) A more problematic issue concerns the inter-pretation of the differential roles of the occipital lobesin naming animals and artifacts The interpretation pro-posed by Martin et al (1996) is that because animals arevisually more complex there is a ldquotop-downrdquo modulationof visual processing to help visual identicationWhether or not this interpretation is correct there areno reports of either category-specic recognition orcategory-specic semantic decits following lesions ofthe left extrastriate cortex Thus the relevance of theobservation that the occipital lobes are more intenselyactivated in naming animals as opposed to artifacts forissues about semantic processing remains obscure Whatis clear however is that different neural mechanisms areinvolved in processing the categories of animate andinanimate objects

Category-Specic Organization ConceptualPerceptual or Both

A nal issue that needs to be addressed here is therelation between object recognition and semantic cate-gory-specic decits Sartori and Job (1988) were therst to report that a patient with a semantic category-specic decit was unable to distinguish between realand chimeric animals EW also showed marked difcul-ties distinguishing between real and unreal animalsHowever the association of a category-specic decit inobject decision tasks with category-specic difcultiesin lexical processing tasks is not a necessary one Thereare reports of patients who show category-specicdecits in naming and comprehension tasks but who arefully able to distinguish real from unreal animals (egLaiacona et al 1997 Sheridan amp Humphreys 1993)Thus category-specic object decision decits dissociatefrom category-specic comprehension performance Apossible implication of these facts is that the category-specic organization of conceptual categories occurs atmultiple levels of processing Specically it could beargued not only that the conceptual system is organizedcategorically but also that the object recognition systemis sensitive to category distinctions In other words cate-gory-specic specialization may be found at both cogni-tive and perceptual processing levels This conclusionaccords well with the view that the categorical organi-zation of conceptual knowledge in the brain reects aneural adaptation in response to evolutionary pressuresWith this view the tness value of the proposed cate-gorical distinction would depend in large measure onour ability to successfully make the correct perceptualdistinctions It would be advantageous therefore forspecialization to occur as early as possible in the objectrecognition system30

Conclusion

We have reported the detailed analysis of the perfor-mance of a brain-damaged subject with a clear-cut cate-gory-specic decit Two features of this subjectrsquosperformance are of crucial interest The decit wasrestricted to the category of animate objects and itinvolved equally visual and functionalassociative knowl-edge of animals This pattern of performance is highlyproblematic for the sensoryfunctional theory of cate-gory-specic decits We have also shown through acritical review of the literature on category-specicdecits that the SFT is without empirical support In-stead the evidence is consistent with the OUCH modelwhich maintains that categorical organization in the se-mantic system emerges from the correlational structureof the properties of members of a category However wehave also argued that the results invite the more intrigu-ing hypothesis that there are different levels of organiza-

Caramazza and Shelton 23

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

tion in the neural system One very basic level of organi-zation reects neural adaptations in response to evolu-tionary pressures for the rapid successful recognition ofanimate (and plant life) objects This is the only truecategorical organization of conceptual (and perhaps per-ceptual) knowledge in the brain In addition however itis possible that there is further structure within thesebroad domains of knowledge We have proposed that thelatter structure is not categorical in form but reects thecorrelational properties of members of semantic catego-ries

METHODS

Subjects

EW is a 72-year-old woman who suffered a left cerebralvascular accident in February 1988 CT scans in Januaryof 1995 revealed a large area of encephlomalacia withinthe left posterior frontal and parietal lobes consistentwith the old infarct (from 1988) At the time of thestroke EW was working in the personnel department ofa government agency She has a high school educationand a degree from a secretarial school (ie approxi-mately 14 years of schooling) EW was rst seen by usin February 1996

EW is uent and produces well-formed coherent sen-tences both in constrained production tasks and spon-taneous speech In response to the ldquoCookie Theftrdquopicture (Goodglass amp Kaplan 1983) she produced thefollowing ldquoThe boy is on the stool getting the cookie jarThe girl is washing dishes and the water is going all overthe oorrdquo

EW does not present with any sentence comprehen-sion impairments and reading of single words is almostperfect EW has signicant problems with both writtenand oral spelling

It rst came to our attention that EW had difcultywith animals when she was asked to name picturesincluded in a screening battery The only pictures shecould not name were pictures of animals EW reportedthat ldquoIrsquom not good with animals They always give metroublerdquo Later we asked EW whether she had problemswith animals because she never had much experiencewith them She responded ldquoWell I did know some thingsabout animals I used to take my kids to the zoo and suchItrsquos worse since I had my stroke Now I have no ideaabout animals at all They [her speech therapists] usedto give me pictures and I told them I couldnrsquot do animalsI canrsquot even think too much about what animals looklikerdquo

Five elderly subjects matched in age and educationlevel to EW participated in the experiments (mean age728 years range 72 to 73 years mean education 124years range 12 to14 years) Not all subjects completedall experiments

Procedures

Visual Naming Task

The picture set from Snodgrass and Vanderwart (1980)was randomized and presented to EW for naming Eachpicture was presented on a separate sheet of paper EWwas asked to provide the name of each picture and ifunable to provide the name to provide any informationpossible She was given an unlimited amount of time torespond to each picture

Five normal control subjects were presented with thecomplete picture set and asked to provide a name foreach picture This was done to determine if certainpictures elicited alternative but acceptable responsesthat may be particular to the specic age and educationlevel of the patient and to determine if the controlsubjects would show a familiarity effect in naming Somepictures were consistently named incorrectly by at leasttwo or more of the control subjects In these cases theyeither provided a superordinate term (eg beetle regbug artichoke reg vegetable) could not produce anyname (eg seahorse reg 2 subjects said ldquocanrsquot think ofthe namerdquo) provided a semantic description (eg cater-pillar reg thing before it changes into a buttery chisel regshaves things) or in one case could not identify thepicture (peach reg canteen fruit ball puffy thing) Therewere a total of 10 items that resulted in misnaming bytwo or more of the control subjects (ant bee y beetlecaterpillar ostrich seahorse peach artichoke chisel)and these items were removed from all the analysesinvolving the Snodgrass and Vanderwart picture set

Sound Identication Task

Sixteen animal sounds and 16 nonanimal sounds weredownloaded from a digitized sound library (SoundEditProcopy) onto an audio tape Presentation order of thesounds was randomized Three young control subjectslistened to each sound played twice in a row and wereasked to identify the sound For most items all threesubjects correctly identied a sound There were severalitems that elicited alternative but acceptable names andthese were considered correct responses The soundswere presented to EW for identication She was in-structed to listen to the sound and to try and identify itShe was told that some of the sounds were from animalsand some were not This task was administered twice toincrease the number of observations

Object Decision Task

This task was developed to examine EWrsquos ability todistinguish between real and unreal animals and objectsusing the same number of stimuli in the animal andnonanimal conditions Also unreal nonanimal items weredeveloped that were very difcult to distinguish fromreal nonanimal items to equate more closely the animal

24 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

and nonanimal stimuli on level of difculty (see exam-ples presented in Figure 1) Thirty animal pictures and30 nonanimal pictures from the Snodgrass and Vander-wart set were spliced with one another to create unrealanimals and objects The object parts were chosen fromitems that were similar visually (and had similar parts)but did not belong together

Part Decision Task

The real and unreal animals and objects used in theObject Decision Task were edited and used in this taskEach ldquobodyrdquo was separated from its real and unrealldquoheadrdquo and arranged on a sheet of paper with the ldquobodyrdquoon the top half of the sheet and the two ldquoheadsrdquo on thebottom half of the sheet of paper (head and body are inquotes because these terms do not apply directly to theobjectsmdashhowever we will refer to the parts as head andbody for ease of reference) Each head was correctlypaired with its body on one trial and incorrectly pairedwith another body on the second trial (eg on one triala dog body was paired with a donkey head and a doghead on another trial a donkey body was paired with adonkey head and a dog head) Examples of animate andinanimate items are presented in Figure 2 Items wereblocked such that a head pair only appeared once ineach block

Visual Processing Tests BORB Tests 7 8 11 and 12

Several tests from the BORB (Riddoch amp Humphreys1993) were administered to EW to assess her ability to

perform complex visual analysis The tests were admin-istered in the standardized manner In all tasks EW waspresented with a target picture at the top of the pageand two probe pictures at the bottom of the pageFor each task EW was required to pick the appro- pri-ate probe picture depending on the instructionsgiven Control data are taken from that reported in theBORB

In the Minimal Feature View Task (Test 7) the targetpresents an object pictured in a standard viewpoint Theprobe pictures represent either the same object from adifferent viewpoint or a different object that is visuallysimilar to the target picture and presented from thesame viewpoint as the matching probe picture For ex-ample the target picture of a bus displays a bus whenviewed from the side and the two probe pictures displaya bus when viewed from the top and a tractor whenviewed from the top Thus the main identifying featureof the target object is typically hidden from view but theshape of the object is relatively maintained The meanfor control subjects was 233 (SD = 20 range 185ndash25)

In the Foreshortened View Task (Test 8) the targetpicture presents an object pictured in a standard view-point and the probe pictures represent either the sameobject from a different viewpoint or a different objectthat is visually similar to the target picture and presentedfrom the same viewpoint as the matching probe pictureFor example the target picture of a car is pictured whenviewed from the side and the two probe pictures displaya car when viewed from the front and a bus whenviewed from the front Thus the main identifying featureof the target object is typically in view but the shape of

Figure 1 Examples of itemsused in the Object Decisiontask Each item was presentedseparately

Caramazza and Shelton 25

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

the object is relatively obscured The mean for controlsubjects was 216 (SD = 28 range 167ndash25)

In the Item Match Task (Test 11) the target presentsan object from some semantic category and the probepictures represent the same object or a different objectfrom the same category For example the target pictureof a tigerrsquos head is presented with the probe pictures ofa tiger viewed from the side and a polar bear viewedfrom the side Although Riddoch and Humphreys (1993)claim that this task cannot be done on the basis of visualfeatures this claim is easily questionable (eg one couldrely on the stripes of the tiger to match the tiger pic-tures) We view this task as another measure of visualprocessing and visual feature matching rather than ameasure of access to stored knowledge

In the Associative Match Task (Test 12) the targetpresents an object that is associated with one of the twoprobe pictures For example the target of a car is pre-sented with the probe pictures of a road and railroadtracks The mean for control subjects was 275 (SD = 24range 21ndash30) There are ve animal pictures on this testand EWrsquos two errors were on two animal trials For thepicture of the milk bottle EW picked the sheep ratherthan the cow and for the picture of the egg EW pickedthe owl rather than the chicken These are clearly seman-tic association errors that appear to result from herdecit comprehending information about animals

Development and Analysis of New Attribute QuestionTasks

A number of attribute question tasks were developed toaddress specic questions regarding EWrsquos category-spe-cic knowledge decit For each of these ve elderly

control subjects completed each task in two ways Sub-jects were rst told to decide whether or not the state-ment about an object was true (eg bears like honeybears are bred for wool gloves have a space for eachnger gloves are worn on the head) After making theirdecision subjects were asked to rate how condent theywere that they knew the answer to the statement on ascale of 1 to 5 with 1 representing ldquojust guessingrdquo and5 representing ldquoextreme condencerdquo This was done toexamine familiarity of the question being asked aboutan item Items were matched as closely as possible onfamiliarity of the concept itself as determined from theSnodgrass and Vanderwart (1980) norms andor the typi-cality ranking from the Battig and Montague (1969) cate-gory norms Items that were unclear to the controlsubjects andor were judged to be correct even thoughthey were created to be incorrect (eg elephants arebrown) were removed from the stimulus set

Both the control subjects and EW completed all theattribute questions associated with each item in eachattribute judgment task For each experiment task devel-opment is described accordingly Data presented in Ta-bles 6 through 10 represent a subset of the attributequestions For each task items in the specic compari-son groups were matched one-to-one on difculty levelof the attribute as determined by the familiarity ratingsgiven by the control subjects For example a comparisonof the perceptual attributes associated with their respec-tive animal and object concept is relevant to the inves-tigation Thus attribute questions in each of these cellsare matched perfectly for difculty level Data are pre-sented this way to control for the inuence of familiarityor difculty on the level of performance however itshould be noted that the pattern of performance is

Figure 2 Examples of itemsused in the Part Decision taskEach item was presented sepa-rately

26 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

identical for both the matched data set and the wholedata set To keep the number of items in each cell at areasonable level we could not match attributes perfectlyfor every specic comparison Note however that thereis little difference in difculty level between all the cells(eg perceptual animate and associative inanimate)

For the rst attribute judgment task we present databroken down by true and false statements This was doneto demonstrate the lack of response bias for EW thatis she performs equally well (or equally poor) on trueand false statements To simplify presentation of the datafor the rest of the tasks performance is collapsed acrosstrue and false statements EWrsquos performance was alwaysexamined for any indication of a response bias but therewas little suggestion of this in any of the judgment tasks

Attribute Property Task 1 Central Attributes Forty ani-mals and 46 inanimate items (representing fruits vegeta-bles clothing and tools) were selected and between 1and 15 attributes about each item was determined Eachitem and attribute specic to the item were given to 10undergraduate students who were asked to judgewhether or not an attribute was characteristic or impor-tant in dening that concept From these judgmentsthree to six attributes that the largest number of subjectsagreed to be important in dening the concept wereused Matching trials consisted of each attribute pairedcorrectly with the corresponding object and nonmatch-ing trials consisted of attributes pseudorandomly as-signed to other items Matching of items resulted in 98visual questions each for animals and objects and 57associative questions each for animals and objects

Attribute Property Task 2 FoodNonfood AnimalsNine food animals (chicken cow crab lobster pig rabbitsalmon tuna turkey) and nine nonfood animals wereselected (dog horse octopus pigeon raccoon robinshark turtle whale) to serve as items in this task (foodand nonfood animals were considered as such for hergeneration) Six visual attributes and six associativefunc-tional attributes were determined for each item based oninformation collected from normal undergraduates re-garding the attributes most associated with specic items(from the task described above) Nonmatching itemswere created by pseudorandomly assigning attributes toother items Five control subjects completed this taskMatched items resulted in 41 questions each for food andnonfood animals in both the visual and associative cellsrespectively

Attribute Property Task 3 GeneralSpecic PropertyJudgments Sixty-ve animals (15 each for birds insectssea animals 20 mammals) and 45 objects (15 each forfruits vegetables buildings) were selected and werematched as best as possible on familiarity (not all itemshad familiarity ratings because they are not all repre-sented in the Snodgrass and Vanderwart set) Items

within each category (eg birds fruit) were the rst 15items listed in the Battig and Montague (1969) categorymembership norms The attributes that were common toall members of a category (eg all animals or all build-ings) and attributes that were common to only somemembers of a category are summarized in Table 11 Be-cause of the number of trials (n = 1165) an equal num-ber of true and false statements were not createdInstead each attribute was asked of each item in a cate-gory The table shows the attributes that were queriedfor each item in each of the four categories testedMatched items for specic attributes resulted in 100visualperceptual questions for both animate and inani-mate items and 150 associativefunctional questions forboth animate and inanimate items

Attribute Property Task 4a Size Judgments Thirty ani-mate pairs and 30 inanimate pairs were developed Onemember of the pair was judged to be larger than thesecond member of the pair although the distinctionrequired a ne discrimination (eg goat-raccoon tomato-pea) Four control subjects completed this task Matcheditems resulted in 18 items in the animate and inanimatecategories respectively

Attributes Property Task 4b Other Shared AttributesSeven attributes that are ldquosharedrdquo between animate andinanimate objects were selected (big small number oflegs surface texture short tall color) and 12 items thathad one of these features were paired with an item nothaving this feature resulting in 42 trials in the animatecondition and 42 trials in the inanimate object Matcheditems resulted in 42 questions in the animal and objectcategories respectively

Attributes Property Task 5 Visible and Not VisibleAttributes Twenty animals were selected and two tofour pictures of these animals were developed Eachpicture represented a different view of the animal suchthat only in one of the pictures showed the experimen-tally relevant visual attributes of the animal representedFor example one picture of a horse might have all fourlegs a tail and a mane another picture of a horse mightonly be a side view of the head Attribute questions weredeveloped for each animal picture that were either rep-resented in the picture or were not represented in thepicture This resulted in 95 attribute questions that wereanswerable based on the information in the picture and65 attribute questions that were not answerable basedon the information in the picture Each animal was testedonly once in a session EW was shown a picture of theanimal (eg horse) and told ldquoThis is a picture of a horseIrsquom going to ask you some questions about horses andyou can use the information in the picture to answerthemrdquo She was then questioned about attributes associ-ated with a horse (eg number of legs tail mane)

Caramazza and Shelton 27

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

Acknowledgments

The work reported here was supported in part by grantNS22201 We thank EW for her generous contribution to oureffort to understand the neural basis for the organization ofconceptual knowledge We also thank Sushant Srinivasan andNina Das for their help in testing control subjects and UpendraMaddenini for help in developing testing materials We aregrateful to Michele Miozzo for many helpful discussions aboutcategory-specic decits and to Ed Smith and Marc Hauser fordetailed and very helpful comments on an earlier version ofthis article Briefer versions of this paper were presented at ameeting of the British Neuropsychology Society (April 1997)a workshop on the neuropsychology of language at the Uni-versity of Michigan (May 1997) and colloquia at Brown Uni-versity (March 1997) and the Aphasia Research Center Boston(April 1997)

Reprint requests should be sent to Alfonso Caramazza Cogni-tive Neuropsychology Laboratory Department of PsychologyWilliam James Hall Harvard University 33 Kirkland St Cam-bridge MA 02138 or via e-mail caramwjhharvardedu

Notes

1 A terminological note As used here the category of livingthings includes both animals and plants the category of ani-mate objects includes only animals Warrington and Shallice(1984) use the term inanimate synonymously with nonlivingWe will restrict the use of inanimate to all objects outside ofthe animal world in other words to mean roughly ldquonot en-

dowed with animal liferdquo In discussing the results on category-specic decits we will initially use the terms living and non-living somewhat imprecisely Thus if we state that a subjecthas selective decit for the living category we do not neces-sarily mean to imply that all subcategories of living things arein fact impaired it might have turned out for example that theimpairment concerned only animals Similarly the claim that asubject is disproportionately impaired with the living categorydoes not imply necessarily that all subcategories of nonlivingthings are equally unimpaired Unless otherwise indicatedliving and nonliving are merely shorthand for predominantlyliving and predominantly nonliving categories In the cognitive neuroscience literature category-specicdecits have typically been discussed in terms of the livingnonliving distinction In this report we will propose that amore accurate characterization of category-specic decits isin terms of the animateinanimate distinction which growsout of evolutionary considerations as well as developmentaland neuropsychological data 2 To be sure there had been intimations of such a possibilityin the neurological literature since Nielsenrsquos (1946) brief reportof two cases who showed disproportionate decits for livingand nonliving things respectively But these reports weremostly anecdotal in their characterization of the supposedlyselective decits Other sporadic reports of category-specicdecits involving one or another conceptual category eitherdid not provide the detailed quantitative analyses necessary toclearly establish the phenomenon (eg Heacutecaen amp Ajuriaguerra1956 Yamadori amp Albert 1973) or presented not-easily explica-ble dissociations (eg the selective sparing of the names ofcountries McKenna amp Warrington 1978) Furthermore al-though the selective decit of body-part names had already

Table 11 Attributes Included in Property Task

General Specic

Category Visual Functional Visual Functional

AnimalMouth Breathe Feathers Lay eggs

Eyes Digest Fur Live in water

4 legs Live on land

Wings Fly

Fruit Skin Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Red Buy canned

Oblong Grow on a vine

Vegetable End to cut off Need water to grow Green Grow in Massachusetts

Need sun to grow Round Buy frozen

Brown Buy canned

Oblong Grow under dirt

Building Large Protect from weather Porch Use for business

Roof Steeple Use for living

Brick Use for religion

28 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

been clearly documented (eg Dennis 1976 Selecki amp Herron1965 Weinstein 1964) discussions of this decit did not spe-cically focus on the possibility that the semantic system mightbe organized categorically Instead body-part naming decitswere typically discussed in relation to disturbances of theldquobody imagerdquomdashautotopagnosia (De Renzi amp Scotti 1970)mdashandconsequently may have been seen as a nontypical semanticdomain Thus it wasnrsquot until Warrington and Shallicersquos (1984)paper that a compelling empirical basis was provided for thepossibility that the semantic system might be organized cate-gorically 3 Over the past several years there have been a number ofreports of category-specic decits in patients with degenera-tive brain disease (see for example Gonnerman AndersenDevlin Kempler amp Seidenberg 1997 Silveri Daniele Giustolisiamp Gainotti 1991) However most of these reports did notcarefully control for various nuisance variables such as differ-ences in familiarity and visual complexity across semantic cate-gories (see below) Furthermore the results are not obtainedreliably and whenever a category-like effect is obtained it israther small by comparison to the effects obtained in the casesreviewed here We will not discuss these reports 4 There has also been a different sort of reluctance againstadopting the proposal that the semantic system might be or-ganized categorically It has been voiced most clearly by Farahand her collaborators (Farah amp McClelland 1991 Farah et al1996) and represents a basic tenet of associationistic accountsof cognition They have argued that the adoption of the viewthat semantic knowledge is organized categorically in the brainwould represent ldquoa signicant departure from everything elsewe know about brain organization according to which subsys-tems are delineated by function or modality but not by seman-tic contentrdquo (Farah et al 1996 p 143) Despite the baldnessof this assertion there is hardly any evidence that speaksdirectly to the issue of how ldquosemantic contentrdquo is representedin the brain And in fact the authors do not provide anyrelevant citations to empirical evidence that would supporttheir contention We will discuss recent neuroimaging resultsthat might be relevant to this issue later in the paper 5 This does not imply that retrieval of nonvisual propertiesfor living things would remain unaffected by damage to visualproperties On the contrary damage to any denitionally im-portant subset of the semantic properties of objects will affectretrieval of other semantic properties Thus damage to thevisual semantic subsystem is also expected to affect retrievalof the functional properties of living things but to a lesserextent See text below for more detailed discussion 6 There are many other studies of category-specic decitthan are considered in this section of our paper Howeverbecause these studies did not explicitly mention the categoriesunder consideration here we are unable to unambiguouslydetermine whether the relevant associationdissociation wasobtained For example Basso et al (1988) Farah et al (19891991) Pietrini et al (1988) Sartori and Job (1988) do not reportperformance for foods 7 We consider later Farah and McClellandrsquos (1991) effort toempirically support the (somewhat different) claim that themembers of the categories of living and nonliving things de-pend differentially on visual and functional attributes for theirmeanings 8 In the literature on category-specic decits the notion ofldquofunctionalrdquo property is used synonymously with ldquononsensoryrdquoproperty For example the typical habitat of an animal wouldbe part of the functional properties of that animal 9 Although the Sartori and Job (1988) are often cited asshowing an association of category- and modality-specic se-mantic decits this attribution may be inaccurate The investi-gation of subject Michelangelo by Sartori and Job focused

principally on his ability to process pictured objects And infact the authors argue that Michelangelorsquos decit may havebeen restricted to the processing of ldquostructural descriptionsrdquofor recognizing objects and not the semantic system itselfNevertheless Michelangelo was not consistently better able toprocess visual as opposed to functional aspects of the mean-ing of living things For example he was 100 correct injudging which of two animals was the larger one10 There are additional difculties with this study that makeits interpretation highly problematic To test whether the sub-ject LA had greater difculty processing the visual or thefunctional attributes of living category items the authors useda naming-to-denition task The denitions stressed either thevisual or the functional properties of an animal However theanimals used in the visual-emphasis denitions were harder toname than those used in the function-emphasis denitions asindicated by LArsquos performance in an independent naming task(Exp C) Thus the alleged disproportionate difculty with vis-ual as opposed to functional attributes of living things (Exp D)cannot be meaningfully interpreted Gainotti and Silveri (1996)acknowledge this problem and report the results of new ex-periments that are supposed to be free of interpretationdifculties These new results are discussed in the main text11 It should be noted that this pattern of performancemdashdifculty in processing only visual attributes of animalsmdashis notcompatible with the Farah and McClelland (1991) version ofthe SFT This version of the theory predicts disproportionatedifculty for visual versus functional attributes but does notpredict complete sparing of functional judgments in the faceof severe naming difculty for living things12 The point here is that KRrsquos performance is not explicableby assuming damage to the semantic system because a conse-quence of such damage would presumably be the productionof nonsystematic errors The systematicity of the errors mightsuggest some type of ldquopsychiatricrdquo disturbance None of thismeans that the case is less interesting It does however raisethe question of whether it is relevant to the issues underconsideration here13 And even if one were to ignore these problems there isthe additional difculty that the SFT does not predict justpoorer performance in processing visual attributes for theliving things category but also for the nonliving things categoryThis prediction clearly follows from the hypothesis that theunderlying cause of the category-specic decit is damage toa visual semantic subsystem that is presumably shared by allconcepts Consequently damage to this subsystem should alsodisproportionately impair performance for visual attributes ofnonliving concepts (though not to the same degree) Howeverthis interaction has not been systematically observed (egGainotti amp Silveri 1996) Thus it does not appear that theinvestigation of differential performance for visual and func-tional attributes of concepts has produced a coherent patternof results on which to base the SFT14 The two subjects studied in the Laiacona Barbarotto ampCapitani (1993) paper were trauma cases raising the possibilitythat aetiology may play a role in determining whether or notknowledge of visual and functional attributes are differentiallyimpaired in subjects with category-specic decits This possi-bility is excluded by their more recent study (Laiacona et al1997) in which they report two new herpes simplex encepha-litis cases with clear category-specic decits for living thingsbut who like the trauma cases show equal levels of perfor-mance for knowledge of visual and functional attributes15 Shallice (personal communication April 1997) has alsoobserved that JBR was equally impaired in processing visualand functional attributes of living and nonliving things16 The notion of modality-specic decit is multiply ambigu-ous One sense of modality-specic refers to a selective decit

Caramazza and Shelton 29

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

of the modality of input or output that is the modality ofpresentation of the stimulus or the modality used for produc-tion of a response In this sense a modality-specic decitmight refer to a subject who for example is disproportionatelyimpaired in processing auditorially presented stimuli Anothersense of modality-specic refers to the type of stimulus orresponse In this sense pictures and written words are differentmodalitiesmdashvisual and verbal respectivelymdasheven though bothare presented visually The third sense of modality-specicrefers to a type of knowledge In this latter sense modalityrefers to the type of properties of objects Thus for example adistinction is drawn between the visual and functional (verbal)attributes of objects Researchers have not always been carefulto distinguish among these senses of modality-specic Unlessotherwise indicated here we will use this term to refer to atype of knowledge17 The notion of ldquodensenessrdquo discussed here is to be distin-guished from the unrelated notion referring to the amount ofinformation one has about a conceptmdashwe have lots of infor-mation about some things and only sparse knowledge aboutothers The latter notion of denseness is also likely to gureinto the probability that a concept will be adversely affectedby brain damage And it may even play a role in the possibilitythat semantic decits may be categorical in nature in thesense that categories for which we only have little knowledgeare more likely to be disproportionately affected by braindamage18 It is important to note that the emphasis being placed hereon domain-specic knowledge systems as the result of evolu-tionary adaptations is not necessarily at odds with the OUCHand SFT hypotheses of category-specic decits It may turnout that the two types of theories provide explanations of thesame phenomenon at different levels of analysis We explorethis possibility in the ldquoDiscussionrdquo section19 Note that the claim is not that the only types of category-specic decits that will be observed will involve the catego-ries of animals plants and artifacts Other category-specictypes of decits may be observed but these will have byhypothesis different causes from those for the major categorieslisted above We return to this issue in the ldquoDiscussionrdquo section20 Once again however as we shall see in the text below thisaccount of category-specic decits does not preclude thepossibility of selective decits restricted to particular modali-ties of access such as visual object recognition versus wordcomprehension21 EW was administered two other object decision tasks Inboth tasks she performed very poorly with animals On Test 10of the BORB (Riddoch amp Humphreys 1993) she scored 70correct for animals versus 94 correct for nonanimals Onanother test with 36 items of which half were real animals andthe other half were unreal animals created by combining twohalves of different animals she scored 72 correct22 Although the terms general and specic attributes arerelated to the concepts of ldquodeningrdquo and ldquocharacteristicrdquo fea-ture (Smith Shoben amp Rips 1974) we use these terms some-what more loosely to capture the fact that some properties aremuch more likely to be shared by members of a categorywhereas others may be specic to one or only a few membersof a category Furthermore the general attributes may notcorrespond to the technically important features (eg egg-laying biped) of a category but to the perceptually and cultur-ally salient ones23 The notions of ldquosharedrdquo or ldquosamerdquo attributes across catego-ries must not be given undue theoretical importance at thispoint That is by using these notions we do not wish to commitourselves to the view that meanings are built up from a set ofsemantic primitives that are shared across semantic domainsIt may turn out that categories share very few if any attribute

concepts Thus for example the attribute ldquohas wingsrdquo (or ldquohasfour legsrdquo ldquohas texture Xrdquo etc) which may be claimed to beshared across animate and inanimate categories may in factcorrespond to different attribute concepts in the two semanticdomains That is perhaps there is no abstract attribute ldquohaswingsrdquo that is shared by say birds and airplanes the attributeldquohas wingsrdquo in the domain of animals might be a differentconcept altogether from the homonymous ldquohas wingsrdquo in thedomain of vehicles24 Farah and McClelland (1991) note that damage to thevisual semantic component of their network model also leadsto some decit on functional questions This result too isunsurprising given that the meaning of a word depends on thewhole set of properties that dene it25 We thank Martha Farah for making the denitions availableto us26 We tested 16 subjects Eight subjects were asked to under-line all sensoryperceptual descriptors and the other eightsubjects were asked to underline all nonsensory (functionalassociative) descriptors for each denition of the set of wordsused by Farah and McClelland (1991)27 It is important to emphasize that if Farah and McClelland(1991) had intended all along to restrict the term functionalto precisely the sense of ldquohaving a functionrdquo an equally seriouscriticism would be raised against the computer simulation Forin this case the dichotomy sensory-functional would fail tocapture the bulk of the nonsensory information we have aboutanimals (as argued in the text above) And since functionalproperties (in the strict sense) do not play a signicant role indistinguishing among animals the computer demonstrationwould have left out just the important nonsensory informationwe have about animals That the narrow sense of functional is not the sense in-tended by proponents of the SFT is clearly indicated by thefact that in experiments in which they investigate the relativeloss of visual and ldquofunctionalrdquo properties they have includedproperties such as carnivore lives in the desert etc (see forexample Farah et al 1989) These properties are not functionalin the strict sense of ldquohaving a functionrdquo28 That is those category-specic decits that are not theresult of uncontrolled factors such as familiarity frequencycomplexity or other idiosyncratic factors concerning the par-ticular histories of individuals with various categories of knowl-edge29 There are reasons for being skeptical of Damasio et alrsquosinterpretation of the functional basis for their patientsrsquo cate-gory-specic naming decits They argue that the functionallocus of decit in their patients is at the level of lexical selec-tion and not at the semantic level They support this claim bynoting that they included for analysis only those naming fail-ures for which it could be ascertained that the patient hadldquocorrectly recognizedrdquo the to-be-named item The criterion forrecognition was that the patient either named the item cor-rectly or provided an adequate description Thus they rea-soned if a patient shows disproportionate naming difculty fora particular semantic category it could be concluded that thisdifculty must arise at a level of processing beyond the seman-tic level since the to-be-named items were presumably cor-rectly recognized The authors identify this postsemantic stageof processing as the level at which lexical selection occursThere are several problems with this conclusion The authors do not report evidence that would allow in-ferences about the integrity of semantic processing in theirpatients Thus for example no data are reported on compre-hension performance the only data reported are those con-cerning naming performance This is unfortunate because toour knowledge all the cases of semantic category-specicdecit in the literature have been reported to have had a decit

30 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

in semantic processing This is certainly the case for patientswith herpes simplex encephalitis who have all been shown tohave had both naming and comprehension category-specicdecits And presumably this would also have been true forthe ve cases of herpes simplex encephalitis included in thesample of patients tested by Damasio et al (1996) (who prob-ably were disproportionately impaired in naming animals) Inother words it seems that the criteria used by the authors forestablishing that the relevant feature of their patientsrsquo namingperformance is a decit restricted to mechanisms of lexicalaccess (as opposed to semantic representations) may havebeen inadequate The latter problem is recognized by the authors but they goon to argue ldquoOur scoring procedure ensures that the defectsreported here pertain to word retrieval rather than to recogni-tion impairments even in subjects who showed defects in bothnaming and recognitionrdquo (Damasio et al 1996 p 500) Thisargument is based on the reasoning that the lexical retrievalfailure observed in the patients is in addition to whateverother difculty they may have had in recognizing specicto-be-named items But this reasoning is suspect Without otherinformation we do not know whether it is only those patientswho showed disproportionate recognitioncomprehensionfailure for the items in a specic category who also showeddisproportionate naming failures in that category Were this thecase we would have grounds for supposing that the locus offunctional decit in these patients probably concerned thesemantic level The mere fact that a patient provides a descrip-tion of an item that cannot be named does not imply that thebasis for the naming failure does not reside at the semanticlevel of processing That is there is little indication that thedescriptions provided by the patients were unambiguousTaken out of context the ldquoappropriaterdquo descriptions actuallymay not clearly describe the to-be-named item There are other problems of interpretation with the resultsof this study Damasio et al (1996) report that they includedfor analysis only those patients who ldquowere able to recognizeat least 50 of items in each categoryrdquo (p 500) Again withoutfurther information it is difcult to interpret the authorsrsquo re-sults because the naming data for different subjects could bebased on radically different subsets of test items depending onwhich items they failed to recognize Another problem concerns the method used to determinethat a patient had a category-specic decit A patient wasclassied as having a category-specic decit if naming perfor-mance was more than two standard deviations below the meanfor the normal controls This means that it is possible that apatient who scored 195 SD below the mean for one categorybut 205 SD below the mean for another category would havebeen classied as having a category-specic decit for thelatter category Unfortunately unlike other reports of category-specic decits the authors do not provide a direct compari-son of performance between categories for each patient withputative category-specic decits Furthermore when theproblems introduced by this criterion are considered inthe context of the scoring procedure used by the authors (theexclusion of an unequal number of trials from different cate-gories for different subjects due to recognition failure) it be-comes extremely difcult to compare the putative cases ofcategory-specic decit reported by Damasio et al (1996) withother cases in the literature And certainly we cannot becondent that their patients represent cases of category-specic lexical as opposed to semantic processing decit30 This speculation may provide a basis for the functionalimaging results that show extrastriate activation for the cate-gory of animals However on the negative side it must be notedthat to our knowledge there are no cases of category-specicagnosias for the categories of animate and inanimate catego-

ries Such decits ought to be observed if there were categori-cal specialization early in the object recognition system Per-haps a possible case demonstrating this is the patient reportedby Sartori and Job (1988)

REFERENCES

Albert M S Butters N amp Levin J (1979) Temporal gradi-ents in the retrograde amnesia of patients with alcoholicKorsakoffrsquos disease Archives of Neurology 36 211ndash216

Allport D A (1985) Distributed memory modular subsys-tems and dysphasia In S K Newman amp R Epstein (Eds)Current perspectives in dysphasia (pp 32ndash60) Edin-burgh Churchill Livingstone

Atran S (1995) Causal constraints on categories and cate-gorical constraints on biological reasoning across culturesIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp205ndash233) NewYork Oxford University Press

Baillargeon R (1993) The object concept revisited New di-rection in the investigation of infantsrsquo physical knowledgeIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 265ndash315) Hillsdale NJ Erlbaum

Basso A Capitani E amp Laiacona M (1988) Progressive lan-guage impairment without dementia A case with isolatedcategory specic semantic defect Journal of NeurologyNeurosurgery and Psychiatry 51 1201ndash1207

Battig W F amp Montague W E (1969) Category norms forverbal items in 56 categories A replication and extensionof the Connecticut category norms Journal of Experimen-tal Psychology Monographs 80 (3 part 2)

Bertenthal B I (1993) Infantsrsquo perception of biomechanicalmotions Intrinsic image and knowledge-based constraintsIn C Granrud (Ed) Visual perception and cognition ininfancy Carnegie Mellon Symposia on Cognition(pp 175ndash214) Hillsdale NJ Erlbaum

Bertenthal B I Proftt D R amp Cutting J E (1984) Infantsensitivity to gural coherence in biomechanical motionsJournal of Experimental Child Psychology 37 213ndash230

Bloom P (1996) Intention history and artifact concepts Cog-nition 60 1ndash29

Caramazza A Hillis A E Rapp B C amp Romani C (1990)The multiple semantics hypothesis Multiple confusionsCognitive Neuropsychology 7 161ndash189

Carey S (1985) Conceptual change in childhood Cam-bridge MA BradfordMIT Press

Carey S (1995) On the origin of causal understanding InD Sperber D Premack amp A J Premack (Eds) Causal cog-nition A multidisciplinary debate (pp 268ndash302) NewYork Oxford University Press

Carey S amp Spelke E (1994) Domain-specic knowledgeand conceptual change In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 169ndash200) New York Cambridge Uni-versity Press

Chomsky N (1980) Rules and representations New YorkColumbia University Press

Chomsky N (1986) Knowledge of language Its natureorigin and use New York Praeger

Damasio H Grabowski T J Tranel D Hichwa R D ampDamasio A R (1996) A neural basis for lexical retrievalNature 380 499ndash505

Dennis M (1976) Dissociated naming and locating of bodyparts after left anterior temporal lobe resection An experi-mental case study Brain and Language 3 147ndash163

Caramazza and Shelton 31

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

De Renzi E amp Lucchelli F (1994) Are semantic systemsseparately represented in the brain The case of living cate-gory impairment Cortex 30 3ndash25

De Renzi E amp Scotti G (1970) Atotopagnosia Fiction or re-ality Archives of Neurology 23 221ndash227

Farah M J Hammond K M Mehta Z amp Ratcliff G (1989)Category-specicity and modality-specicity in semanticmemory Neuropsychologia 27 193ndash200

Farah M J amp McClelland J L (1991) A computationalmodel of semantic memory impairment Modality spe-cicity and emergent category specicity Journal of Ex-perimental Psychology General 120 339ndash357

Farah M J McMullen P A amp Meyer M M (1991) Can rec-ognition of living things be selectively impaired Neuropsy-chologia 29 185ndash193

Farah M J Meyer M M amp McMullen P A (1996) The liv-ingnonliving dissociation is not an artifact Giving ana priori implausible hypothesis a strong test CognitiveNeuropsychology 13 137ndash154

Farah M J amp Wallace M A (1992) Semantically-boundedanomia Implications for the neural implementation ofnaming Neuropsychologia 30 609ndash621

Funnell E amp De Mornay Davies P (1997) JBR A reassess-ment of concept familiarity and a category-specic disor-der for living things Neurocase 2 461ndash474

Funnell E amp Sheridan J S (1992) Categories of knowledgeUnfamiliar aspects of living and nonliving things Cogni-tive Neuropsychology 9 135ndash153

Gaffan D amp Heywood C A (1993) A spurious category-specic visual agnosia for living things in normal humansand nonhuman primates Journal of Cognitive Neurosci-ence 5 118ndash128

Gainotti G amp Silveri M C (1996) Cognitive and anatomicallocus of lesion in a patient with a category-specic seman-tic impairment for living beings Cognitive Neuropsychol-ogy 13 357ndash389

Gainotti G Silveri M C Daniele A amp Giustolisi L (1995)Neuroanatomical correlates of category-specic semanticdisorders A critical survey In R A McCarthy (Ed) Seman-tic knowledge and semantic representations MemoryVol 3 Issues 3 amp 4 (pp 247ndash264) Hove EnglandErlbaum Taylor amp Francis

Gelman R (1990) First principles organize attention to andlearning about relevant data Number and the animate-inanimate distinction as examples Cognitive Science 1479ndash106

Gelman R amp Brenneman K (1994) First principles can sup-port both universal and culture-specic learning aboutnumber and music In L A Hirschfeld amp S A Gelman(Eds) Mapping the mind Domain specicity in cogni-tion and culture (pp 369ndash390) New York CambridgeUniversity Press

Gelman R Durgin F amp Kaufman L (1995) Distinguishingbetween animates and inanimates Not by motion aloneIn D Sperber D Premack amp A J Premack (Eds) Causalcognition A multidisciplinary debate (pp 150ndash184) NewYork Clarendon PressOxford University Press

Gelman S amp Coley J D (1990) The importance of knowinga dodo is a bird Categories and inferences in 2-year-oldchildren Developmental Psychology 26 796ndash804

Gonnerman L M Andersen E S Devlin J T Kempler Damp Seidenberg M S (1997) Double dissociation of seman-tic categories in Alzheimerrsquos disease Brain and Lan-guage 57 254ndash279

Goodglass H amp Kaplan E (1983) The assessment of apha-sia and related disorders 2nd ed Philadelphia PA Lea ampFebiger

Hart J Berndt R S amp Caramazza A C ( 1985) Category-specic naming decit following cerebral infarction Na-ture 316 439ndash440

Hart J amp Gordon B (1992) Neural subsystems for objectknowledge Nature 359 60ndash64

Hauser M D (in press) The functional properties of artifactsA nonhuman primatersquos view Cognition

Heacutecaen H amp Ajuriaguerra de J (1956) Agnosie visuellepour les objets inanimes par lesion unilaterale gauche Re-vue Neurologique 94 222ndash223

Hillis A E amp Caramazza A (1991) Category-specic namingand comprehension impairment A double dissociationBrain 114 2081ndash2094

Hillis A E Rapp B amp Caramazza A (1995) Constrainingclaims about theories of semantic memory More on uni-tary versus multiple semantics Cognitive Neuropsychol-ogy 12 175ndash186

Hirschfeld L A amp Gelman S A (Eds) (1994) Mapping themind Domain specicity in cognition and culture NewYork Cambridge University Press

Humphreys G W amp Riddoch M J (1987) On telling yourfruit from your vegetables A consideration of category-specic decits after brain damage Trends in Neurosci-ence 4 145ndash148

Keil F C (1989) Concepts kinds and cognitive develop-ment Cambridge MA MIT Press

Keil F C (1994) The birth and nurturance of concepts bydomains The origins of concepts of living things In L AHirschfeld amp S A Gelman (Eds) Mapping the mind Do-main specicity in cognition and culture (pp 234ndash254)New York Cambridge University Press

Kurbat M A (1997) Can the recognition of living thingsreally be selectively impaired Neuropsychologia 35 813ndash827

Laiacona M Barbarotto R amp Capitani E (1993) Perceptualand associative knowledge in category specic impair-ment of semantic memory A study of two cases Cortex29 727ndash740

Laiacona M Barbarotto R Trivelli C amp Capitani E (1993)Category specic semantic defects A standardised testwith normative data Archivio di Psicologia Neurologiae Psichiatria 54 209ndash248

Laiacona M Capitani E amp Barbarotto R (1997) Semanticcategory dissociations A longitudinal study of two casesCortex

Leslie A M (1982) The perception of causality in infantsPerception 11 173ndash186

Leslie A M (1984) Spatiotemporal continuity and the per-ception of causality in infants Perception 13 287ndash305

Leslie A M (1988) The necessity of illusion Perception andthought in infancy In L Weiskrantz (Ed) Thought with-out language A Fyssen Foundation symposium (pp 185ndash210) Oxford England Clarendon PressOxford UniversityPress

Leslie A M amp Keeble S (1987) Do six-month old infantsperceive causality Cognition 25 265ndash288

Liberman A M amp Mattingly I G (1989) A specialization forspeech perception Science 243 489ndash494

Mandler J M (1992) How to build a baby II Conceptualprimitives Psychological Review 99 587ndash604

Mandler J M (1994) Precursors of linguistic knowledgePhilosophical Transactions of the Royal Society of Lon-don 346 63ndash69

Mandler J M Bauer P J amp McDonough L (1991) Separat-ing the sheep from the goats Differentiating global catego-ries Cognitive Psychology 23 263ndash298

32 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

Mandler J M amp McDonough L (1993) Concept formationin infancy Cognitive Development 8 291ndash318

Markman E M (1989) Categorization and naming in chil-dren Problems of induction Cambridge MA MIT Press

Martin A Wiggs C L Ungerleider L G amp Haxby J V(1996) Neural correlates of category-specic knowledgeNature 379 649ndash652

McCarthy R A amp Warrington E K (1988) Evidence for mo-dality-specic meaning systems in the brain Nature 334428ndash430

McClelland J L amp Rumelhart D E (1986) Parallel distrib-uted processing Explorations in the microstructures ofcognition Volume 2 Psychological and biological mod-els Cambridge MA MIT Press

McKenna P amp Warrington E K (1978) Category specicnaming preservation A single case study Journal of Neu-rology Neurosurgery and Psychiatry 43 781ndash788

McRae K de Sa V R amp Seidenberg M S (1997) On the na-ture and scope of featural representations for word mean-ing Journal of Experimental Psychology General 12699ndash130

Nielsen J M (1946) Agnosia apraxia aphasia Their valuein cerebral localisation 2nd ed New York Harper

Perani D Cappa S F Bettinardi V Bressi S Gorno-TempiniM Matarrese M Fazio F (1995) Different neural systemsfor the recognition of animals and man-made toolsNeuroreport 6 1637ndash1641

Pietrini V Nertempi P Vaglia A Revello M G Pinna V ampFerro-Milone F (1988) Recovery from herpes simplex en-cephalitis Selective impairment of specic semantic cate-gories with neuroradiological correlation Journal ofNeurology Neurosurgery and Psychiatry 51 1284ndash1293

Pinker S amp Bloom P (1990) Natural language and natural se-lection Behavioral Brain Sciences 13 707ndash784

Powell J amp Davidoff J (1995) Selective impairments of ob-jects knowledge in a case of acquired cortical blindnessMemory 3 435ndash461

Premack D (1990) The infantrsquos theory of self-propelled mo-tion Cognition 36 1ndash16

Quinn P C amp Eimas P D (1996) Perceptual organizationand categorization in young infants In C Rovee-Collier ampL P Lipsitt (Eds) Advances in infancy research Vol 10(pp 1ndash36) Norwood NJ Ablex

Rapp B C Hillis A E amp Caramazza A C (1993) The roleof representations in cognitive theory More on multiplesemantics and the agnosias Cognitive Neuropsychology10 235ndash249

Riddoch M J amp Humphreys G W (1993) Visual aspects ofneglect dyslexia In D W Willows R S Kruk amp E Corcos(Eds) Visual processes in reading and reading disabili-ties (pp 111ndash136) Hillsdale NJ Erlbaum

Riddoch M J Humphreys G W Coltheart M amp Funnell E(1988) Semantic systems or system Neuropsychologicalevidence re-examined Cognitive Neuropsychology 5 3ndash25

Rosch E (1973) On the internal structure of perceptual andsemantic categories In T E Moore (Ed) Cognitive devel-opment and the acquisition of language (pp 111ndash144)New York Academic Press

Rosch E (1975) Cognitive representations of semantic cate-gories Journal of Experimental Psychology General104 192ndash233

Rosch E Mervis C B Gray W D Johnson D M amp Boyes-Braem P (1976) Basic objects in natural categories Cogni-tive Psychology 8 382ndash439

Rozin P amp Schull J (1988) The adaptive-evolutionary point

of view in experimental psychology In R C Atkinson R JHerrnstein G Lindzey amp R D Luce (Eds) Stevensrsquo hand-book of experimental psychology Vol 1 Perception andmotivation Vol 2 Learning and cognition (pp 503ndash546)New York Wiley

Sacchett C amp Humphreys G W (1992) Calling a squirrel asquirrel but a canoe a wigwam A category-specic decitfor artifactual objects and body parts Cognitive Neuropsy-chology 9 73ndash86

Saffran E M amp Schwartz M F (1994) Of cabbages andthings Semantic memory from a neuropsychological per-spectvemdashA tutorial review In C Umilta amp M Moscovitch(Eds) Attention and performance 15 Conscious andnonconscious information processing (pp 507ndash536)Cambridge MA MIT Press

Sartori S amp Job R (1988) The oyster with four legs Aneuropsychological study on the interaction of visual andsemantic information Cognitive Neuropsychology 5 105ndash132

Sartori G Miozzo M amp Job R (1993) Category-specicnaming impairments Yes Quarterly Journal of Experi-mental Psychology 46A 489ndash504

Selecki B R amp Herron J T (1965) Disturbances of the ver-bal body image A particular syndrome of sensory aphasiaJournal of Nervous and Mental Disease 147 42ndash52

Shallice T (1988) Specialisation within the semantic systemCognitive Neuropsychology 5 133ndash142

Sheridan J amp Humphreys G W (1993) A verbal-semanticcategory-specic recognition impairment CognitiveNeuropsychology 10 143ndash184

Silveri M C Daniele A Giustolisi L amp Gainotti G (1991)Dissociation between knowledge of living and nonlivingthings in dementia of the Alzheimerrsquos type Neurology 41545ndash546

Silveri M C amp Gainotti G (1988) Interaction between vi-sion and language in category-specic impairment Cogni-tive Neuropsychology 5 677ndash709

Sirigu A Duhamel J R amp Poncet M (1991) The role of sen-sorimotor experience in object recognition A case of mul-timodal agnosia Brain 114 2555ndash2573

Skinner B F (1957) Verbal behavior New York Appleton-Century-Crofts

Smith E E Shoben E J amp Rips L J (1974) Structure andprocess in semantic memory A featural model for seman-tic decisions Psychological Review 81 214ndash241

Snodgrass J amp Vanderwart M (1980) A standardised set of260 pictures Norms for name agreement familiarity andvisual complexity Journal of Experimental PsychologyHuman Learning and Memory 6 174ndash215

Spelke E S (1988) The origins of physical knowledge InL Weiskrantz (Ed) Thought without language A FyssenFoundation symposium (pp 168ndash184) Oxford EnglandClarendon PressOxford University Press

Spelke E S Phillips A amp Woodward A L (1995) Infantsrsquoknowledge of object motion and human action In D Sper-ber D Premack amp A J Premack (Eds) Causal cognitionA multidisciplinary debate (pp 44ndash78) New York Claren-don PressOxford University Press

Sperber D (1994) The modularity of thought and theepidemiology of representations In L A Hirschfeld amp S AGelman (Eds) Mapping the mind Domain specicity incognition and culture (pp39ndash67) New York CambridgeUniversity Press

Sperber D Premack D amp Premack A J (1995) Causal cog-nition A multidisciplinary debate New York ClarendonPressOxford University Press

Stewart F Parkin A J amp Hunkin N M (1992) Naming im-

Caramazza and Shelton 33

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1

pairments following recovery from herpes simplex en-cephalitis Category-specic Quarterly Journal of Experi-mental Psychology 44A 261ndash284

Warrington E K (1981) Concrete word dyslexia BritishJournal of Psychology 72 175ndash196

Warrington E K amp McCarthy R (1983) Category specicaccess dysphasia Brain 106 859ndash878

Warrington E K amp McCarthy R (1987) Categories of

knowledge Further fractionations and an attempted inte-gration Brain 110 1273ndash1296

Warrington E K amp Shallice T (1984) Category specic se-mantic impairments Brain 107 829ndash854

Weinstein S (1964) Decits concomittant with aphasia orlesions of either hemisphere Cortex 1 154ndash169

Yamadori A amp Albert M L (1973) Word category aphasiaCortex 9 112ndash125

34 Journal of Cognitive Neuroscience Volume 10 Number 1