17. A. H. Bass, C. W. Clark, in Springer Handbook ofAuditory Research, Vol. 16, Acoustic Communication,A. M. Simmons, R. R. Fay, A. Popper, Eds. (Springer-Verlag, New York, NY, 2003), pp. 15–64.

18. M. L. Fine, M. L. Lenhardt, Comp. Biochem. Physiol. A76, 225 (1983).

19. J. R. McKibben, A. H. Bass, J. Comp. Physiol. A 187,271 (2001).

20. J. A. Sisneros, P. M. Forlano, R. Knapp, A. H. Bass, Gen.Comp. Endocrinol. 136, 101 (2004).

21. Materials and methods are available as supplementalmaterial on Science Online.

22. J. M. Goldberg, P. B. Brown, J. Neurophysiol. 32, 613(1969).

23. J. H. Zar, Biostatistical Analysis (Prentice Hall, UpperSaddle River, NJ, ed. 4, 1999).

24. A. E. Stenberg, H. Wang, L. Sahlin, M. Hultcrantz,Hear. Res. 136, 29 (1999).

25. A. E. Stenberg et al., Hear. Res. 157, 87 (2001).26. P. M. Forlano, D. L. Deitcher, D. A. Myers, A. H. Bass,

J. Neurosci. 21, 8943 (2001).27. M. Hultcrantz, A. E. Stenberg, A. Fransson, B. Canlon,

Hear. Res. 143, 182 (2000).28. A. R. Palmer, I. J. Russell, Hear. Res. 24, 1 (1986).29. C. Rose, T. F. Weiss, Hear. Res. 33, 151 (1988).30. T. F. Weiss, C. Rose, Hear. Res. 33, 167 (1988).31. K. Ramanathan, P. A. Fuchs, Biophys. J. 82, 64 (2002).32. S. Yovanof, A. S. Feng, Neurosci. Lett. 36, 291 (1983).33. K. E. Elkind-Hirsch, E. Wallace, L. R. Malinak, J. F.

Jerger, Otolaryngol. Head Neck Surg. 110, 46 (1994).34. M. Haggard, J. B. Gaston, Br. J. Audiol. 12, 105 (1978).35. Research support from NIH (DC00092 to A.H.B.,

1F32DC00445 to J.A.S, and 5T32MH15793 to P.M.F).We thank M. Marchaterre, G. Calliet and the MossLanding Marine Laboratory, and the University ofCalifornia’s Bodega Marine Laboratory for logisticalsupport; and the Bass lab discussion group (especiallyM. Weeg and M. Kittelberger), J. Goodson, R. Hoy, K.Reeve, N. Segil, and P. Sherman for helpful commentson the text.

Supporting Online Materialwww.sciencemag.org/cgi/content/full/305/5682/404/DC1Materials and MethodsFig. S1References

26 February 2004; accepted 28 May 2004

Cognitive Imitation inRhesus Macaques

Francys Subiaul,1* Jessica F. Cantlon,3 Ralph L. Holloway,1

Herbert S. Terrace2,4*

Experiments on imitation typically evaluate a student’s ability to copy somefeature of an expert’s motor behavior. Here, we describe a type of observationallearning in which a student copies a cognitive rule rather than a specific motoraction. Two rhesus macaques were trained to respond, in a prescribed order, todifferent sets of photographs that were displayed on a touch-sensitive monitor.Because the position of the photographs varied randomly from trial to trial,sequences could not be learned by motor imitation. Both monkeys learned newsequencesmore rapidly after observing an expert execute those sequences thanwhen they had to learn new sequences entirely by trial and error.

Can a monkey do what a monkey sees? Formore than a century, scientists have tried, withlittle success, to formulate objective answers tothis deceptively simple question. Measures ofwhat a student sees while observing an expertperform a task have been poorly defined, ashave the criteria for determining which actionscount as imitative and which can be explainedby the principles of conditioning. These prob-lems reflect definitions of imitation that haverelied exclusively on motor tasks. For example,in 1898, Thorndike defined imitation as“learning to do an act from seeing it done”(1). A half-century later, Thorpe proposed amore behavioral definition: “copying anovel or otherwise improbable act” (2).Although Thorndike’s and Thorpe’s defini-tions of imitation have since been qualifiedand elaborated (3–5), neither has been su-perseded. As a consequence, most researchon imitation has focused exclusively onwhat a subject does at the expense of de-termining what the subject knows.

Here we describe an example of cognitiveimitation, a type of observational learning inwhich a naı̈ve student copies an expert’s useof a rule—for example, learning someone’spassword at an ATM by looking over theuser’s shoulder. Because the observer alreadyknows how to enter numbers on the keypad,no motor learning is necessary. The distinc-tion between cognitive and motor imitationis based on the same logic that is used todifferentiate cognitive and motor learningin asocial settings (6 ). In the former, thesubject must learn to represent externalevents in their absence—for example, re-membering someone’s password. In the lat-ter, an external event is available as a cuefor the response in question—for example,an expert’s motor behavior.

To investigate cognitive imitation, wetrained monkeys to execute simultaneouschains, a task in which the subject is requiredto learn a cognitive rule rather than specificmotor actions. The task requires subjects torespond, in a prescribed order, to photographsthat are displayed simultaneously on a touch-sensitive monitor (Fig. 1A) (7, 8). Randomvariation of the positions of the photographsfrom trial to trial ensures that the subjectcannot use a particular motor sequence toexecute the task (Fig. 1B) (9). Eliminatingthat possibility was critical; many previouslyreported instances of imitation in nonhuman

primates have been criticized because theymay be interpreted as instances of individuallearning triggered by the mere presence of aconspecific [social facilitation (10, 11)] or bytheir interaction with a particular object and/or behavior in a particular location [stimulus/local enhancement (2–4)] (12).

Simultaneous chains are typically learnedby trial and error from feedback that followseach response, correct or incorrect. Correctresponses are followed by brief (0.5 s) visualand auditory feedback; errors are followed bya variable (5 to 10 s) time-out, during whichthe screen is dark. Subjects received a foodreward only after they responded correctly toall four items on the monitor (A3 B3 C3D) (9). A trial ends either when the subjectresponds incorrectly to an item or when thesubject responds correctly to all of the itemson the screen. On a four-item list, the prob-ability of a subject guessing the correct se-quence on the first trial and thereby earning afood reward is 1/4! � 0.04.

In the current study, two monkeys wereeach provided with the opportunity to learnnew lists by cognitive imitation rather than bytrial and error. On those lists, one monkeywas designated as the “expert,” the other asthe “student.” The expert had previouslylearned to execute the target list at a highlevel of proficiency. The student had no priorexperience with the target list but was al-lowed to observe the expert execute that listbefore testing (13). Learning a list in thismanner is much more difficult than learningsomeone’s password at an ATM by lookingover the user’s shoulder, because on an ATMthe spatial positions of the number buttonsnever change.

Our subjects were two male rhesus ma-caques, Horatio and Oberon. Both subjectshad acquired considerable expertise at learn-ing lists by trial and error in previous exper-iments (8). In the present study, subjectslearned to execute 70 different four-item listsof arbitrarily selected photographs in two ad-jacent sound-attenuated chambers. The inte-rior walls of each chamber contained a win-dow made of tempered glass. When anopaque partition was placed between the

1Department of Anthropology, 2Department of Psy-chology, Columbia University, New York, NY 10027,USA. 3Department of Psychological and Brain Scienc-es, Duke University, Durham, NC 27708, USA. 4NewYork State Psychiatric Institute, 1051 Riverside Drive,New York, NY 10032, USA.

*To whom correspondence should be addressed. E-mail: subiaul@aol.com (F.S.); terrace@columbia.edu(H.S.T.)

R E P O R T S

www.sciencemag.org SCIENCE VOL 305 16 JULY 2004 407

booths, each glass wall functioned as a mir-ror. When the partition was removed, sub-jects had a full view of one another (9).

In experiment 1, each subject was testedon 30 four-item lists. Fifteen of those listswere collected in isolation with the partitionbetween the chambers in place (baselinecondition). Baseline performance provided ameasure of trial-and-error learning. On theremaining 15 lists, the partition was removed(social-learning condition). This allowed anaı̈ve monkey (the student) to observe anexperienced monkey (the expert) executethe list on which the student would betested. Baseline and social-learning listswere alternated during successive sessionsto balance any list-learning expertise thatsubjects might develop while learning newlists under each condition (9).

Under the social-learning condition, theexpert and the student were placed in theirrespective chambers at the same time be-fore the start of each session. The expertperformed a list on which he had beenovertrained [mean accuracy for Horatio �75.5%; Oberon � 78.7%] (13). The studentwas introduced to that same list during twosuccessive blocks of 20 trials. During thefirst block of 20 trials, the expert executedthe overlearned list (observation period).Throughout this block the student’s moni-tor was dark and inactive. That arrange-ment allowed the student to observe, butnot perform, the sequence that the expertwas executing in the adjacent chamber.During the second block of 20 trials (testperiod), the student’s monitor was activat-ed. This was the student’s first opportunityto respond to the new list items. The onsetsof each of the expert’s and the student’strials were completely independent. Thestudent and the expert worked side by sidethroughout the test period, in full view ofeach other, until the student completed hisblock of 20 trials (9).

A monkey capable of cognitive imitationshould acquire a new list more rapidly whenwatching an expert execute that list thanwhen learning a new list entirely by trial anderror. Our measure of cognitive imitation wasthe number of responses a subject made on anew list before completing his first trial cor-rectly. This is a very sensitive measure ofcognitive imitation because, after the firstcorrect trial, a subject’s performance may beinfluenced by cognitive imitation, by trial anderror, or by both factors.

As seen in Fig. 2A, Horatio and Oberonbenefited substantially from observing anexpert execute a list before being tested.Subjects made significantly fewer respons-es before completing their first trial cor-rectly under the social-learning conditionthan under the baseline condition. That dif-ference suggests that students learned someof the new list items vicariously by moni-toring the responses of the expert duringthe social-learning condition.

To justify that conclusion, it is neces-sary to control for two factors that mayhave favored list learning under the social-learning condition. In experiment 2 wesought to control for nonsocial learning. Inthis instance, a student could benefit fromthe social-learning condition even if he ig-nored the presence of the expert in theadjacent chamber. To learn the serial posi-tion of items in a new list, the student onlyneeded to attend to the visual and auditoryfeedback that followed each of the expert’scorrect responses. In experiment 3, wesought to control for social facilitation thatcould have resulted from the mere presenceof the expert monkey in the adjacent cham-ber (10, 11). Under this scenario, socialfacilitation would have increased the stu-dent’s motivation to attend to the conse-quences of responding to each list item. Inexperiments 2 and 3, students had the sameview of the adjoining chamber that they did

under the social-learning condition in ex-periment 1. Each session consisted of a20-trial observation block followed by a20-trial test block.

In experiment 2, the chamber that waspreviously occupied by the expert monkeywas empty and a computer simulated an ex-pert’s performance on the list on which thestudent was tested (computer-feedback con-dition). In experiment 3, the expert and thestudent worked side by side on differentlists (social-facilitation condition). Subjectslearned 20 new lists in each experiment: 10under one of the control conditions and 10under the baseline condition (9).

Neither control condition enhanced listlearning. The number of responses studentsneeded to complete their first correct trial underthe social-facilitation and the computer-feedback conditions did not differ from thenumber of responses needed during thebaseline conditions (9).

Having established that the social-learningcondition was the only condition under whichlist learning was enhanced, we sought toclarify what the student learned from theexpert. From experiment 1, we know that asubject in the social-learning condition didnot learn the positions of all of the items byobserving an expert execute a new list. If thatwere the case, the student would have need-ed, on average, only four responses to com-plete his first correct trial (Fig. 2A).

What the student gleaned from the ex-pert’s performance was revealed by an item-by-item analysis of the relative frequency of acorrect response at each position of the se-quence before the completion of the firstcorrect trial on a new list. This analysis re-vealed that, in the social-learning condition,Horatio and Oberon learned the ordinal posi-tion of at least two list items. Horatio’s accu-racy when responding to items A and D andOberon’s accuracy when responding to itemsB and C exceeded, by at least 20%, their

Fig. 1. Simultaneouschaining task. (A)Sample of four-itemlist of arbitrary pic-tures. (B) Example ofhow list items (pic-tures) change spatialconfiguration fromtrial to trial.

R E P O R T S

16 JULY 2004 VOL 305 SCIENCE www.sciencemag.org408

accuracy when responding to items in thesepositions under the baseline and the twocontrol conditions (9).

At this stage of our research, we attach noimportance to our subjects’ idiosyncratic se-lection of the items learned while observingan expert execute a list. Those differencesnotwithstanding, the specific ordinal knowl-edge that Horatio and Oberon acquired asstudents was equally effective in minimizingthe overall number of errors in the social-learning condition. Knowledge of the ordinalpositions of any two items makes it easier toinfer the ordinal position of the remainingitems by trial and error.

It remains to be seen whether a studentcould learn a new list without making anyerrors by observing an expert execute thatlist. The fact that Horatio and Oberon did notachieve that level of expertise should not,however, detract from the threefold implica-tion of the cognitive imitation that they did

display. Foremost, Horatio and Oberon’s per-formance as students in the social-learningcondition demonstrates cognitive imitation inan animal. Second, their performance chal-lenges the widely held view that apes are theonly animal species capable of learning byimitation (4, 5, 14–16). Third, Horatio andOberon’s performance falls outside the scopeof all current theories of social learning (2–5,12, 17–24).

The ability of Horatio and Oberon to ac-quire ordinal information by observing an ex-pert execute a list stands in strong contrast tothe failure of other experiments investigatingimitation in monkeys (21). The current experi-ment differs from previous studies in manyrespects. Of greatest importance, our paradigmallows for the separation of motor and cognitiverules, the execution of which might contributeindependently to imitation learning. Indeed, thisis the only experiment on imitation of which weare aware in which no motor learning wasnecessary. The use of a familiar motor taskthroughout testing, in this instance the simulta-neous chaining paradigm, also made it possibleto obtain multiple observations of imitationfrom the same subject.

The simultaneous chaining paradigm alsomade it possible to demonstrate evidence ofcognitive imitation even when a subject didnot reproduce a list perfectly (table S2). Bycontrast, experiments on motor imitationmust focus on a single trial. Failure to repro-duce the expert’s performance on the firsttrial counts as a negative result because, onsubsequent trials, it is not possible to separatewhat was learned by observation from whatwas learned by trial and error. An equallyserious problem is the subject’s level of mo-tor sophistication. Consider, for example, theoutcome of an experiment, like this one, inwhich progress on a cognitive task presup-poses knowledge of the motor task. The like-lihood that subjects could learn either type oftask by imitation is nil.

Theories of stimulus or local enhancementcannot explain how Horatio and Oberon ac-quired ordinal knowledge of at least two itemson social-learning lists. At best, those theoriescan offer an account of how a student mightlearn the first or the last item of a new listbecause these items would be the most salient.Under this scenario, the expert would draw thestudent’s attention to one of these two items.The student would then search for that item onhis own video monitor (while ignoring theremaining items on the screen, with the addeddifficulty that the item’s location differs fromthe location on the expert’s screen). Theoriesof stimulus or local enhancement cannot, how-ever, explain how students could acquireknowledge of the ordinal positions of items Bor C because they make no provision for learn-ing serial rules.

Theories of social facilitation and stimu-

lus enhancement would predict, respectively,more rapid list learning under the social-facilitation and the computer-feedback con-ditions than under the baseline condition.None occurred. Theories of emulation learn-ing [e.g., (4, 5, 16, 17, 24)] cannot explain thetype of cognitive imitation measured herebecause the simultaneous chaining paradigmdoes not provide any “affordances” or anycausal relationship between individual listitems. Because all new lists consisted of ar-bitrarily related pictures, subjects could notuse a general ordering rule between lists.Instead, subjects had to develop a uniqueordering rule to execute each new list.

Our evidence of cognitive imitation inmonkeys is consistent with recent hypoth-eses about different “levels” of imitation[e.g., (14, 15, 18, 25–27 )]. For example,Whiten (25) and Byrne (26) have each ar-gued that a student may copy specific actionsof a model (“action-level imitation”) or that astudent may copy the underlying structureand/or goal of observed motor movements(“program-level imitation”). In this experi-ment, the program our monkeys imitated wasone that allowed them to identify the ordinalposition of new list items.

Having empirically isolated cognitiveimitation from motor imitation, we are leftwith many questions. First, although sub-jects that fail motor imitation tasks maysucceed on cognitive imitation tasks, wecannot state the necessary and sufficientconditions for cognitive imitation to occur.Second, little can be said about either theevolutionary history of motor and cognitiveimitation or their underlying neural mech-anisms. As a result, we cannot hypothesizeabout the extent to which other species maylearn by cognitive imitation.

There are, however, two findings— onefrom this experiment, and one from exper-iments on responses of individual cellsfrom a monkey’s cortex—that suggestsome strategies for addressing these ques-tions. In this experiment, the expert’s eye-hand coordination, as it moved from oneitem to the next on the same list that waspresented to the student, may have recruit-ed the student’s attention to the ordinal po-sition of those items. That aspect of the so-cial-learning condition was absent in both thecomputer-feedback and social-facilitationconditions. The salience of the expert’s ac-tions while responding to particular items inthe social-learning condition may be similarto that observed in experiments that reportedthe firing of specific neuron populations inthe inferior frontal and medial temporal lobesof monkeys that observed intentional move-ments executed by a trainer or by anothermonkey (28, 29). It would, therefore, be ofinterest to explore the extent to which thoseneurons contribute to cognitive imitation.

Fig. 2. (A) Summary data of experiment 1:cognitive imitation [Horatio: t(29) � 8.20, P �0.001; Oberon: t(29) � 9.39, P � 0.001, two-tailed paired-samples t test]. (B) Summary dataof experiment 2: computer-generated feedback[Horatio: t(9) � –1.11, P � 0.30; Oberon:t(9) � 0.28, P � 0.78 (two-tailed paired-sam-ples t test)]. (C) Summary data of experiment 3:social facilitation [Horatio: t(9) � 0.34, P �0.75; Oberon: t(9) � –0.11, P � 0.92 (two-tailed paired-samples t test)].

R E P O R T S

www.sciencemag.org SCIENCE VOL 305 16 JULY 2004 409

References and Notes1. E. Thorndike, Psychol. Rev. Monogr. Suppl. 2, 79(1898).

2. W. Thorpe, Learning and Instinct in Animals (Methuen,London, 1956), p. 122.

3. B. Galef, in Social Learning: Psychological and Biolog-ical Perspectives, T. Zentall, B. Galef, Eds. (Erlbaum,Hillsdale, NJ, 1988), pp. 3–28.

4. M. Tomasello, J. Call, Primate Cognition (Oxford Univ.Press, New York, 1997).

5. A. Whiten, R. Ham, in Advances in the Study ofBehavior, P. Slater, J. Rosenblatt, C. Beer, M. Milinsky,Eds. (Academic Press, New York, 1992), vol. 21, pp.239–283.

6. H. Terrace, in Animal Cognition, H. Roitblat, T. Bever, H.Terrace, Eds. (Erlbaum, Hillsdale, NJ, 1984), pp. 7–28.

7. H. Terrace, in Quantitative Analyses of Behavior: Dis-crimination Processes, M. Commons, R. Herrnstein, A.Wagner, Eds. (Ballinger, Cambridge, MA, 1984), pp.115–138.

8. H. Terrace, L. K. Son, E. Brannon, Psychol. Sci. 14, 66(2003).

9. See supporting data at Science Online.10. D. Clayton, Q. Rev. Biol. 53, 373 (1978).11. R. B. Zajonc, Science 149, 106 (1965).12. Stimulus, local enhancement, and social facilita-

tion are terms that refer to specific instances ofindividual learning that are triggered by the activ-ity of a conspecific. Stimulus and local enhance-ment occur because the model’s behavior attractsan onlooker’s attention toward some object orsome activity in a location. Social enhancementrefers to an increase in attention and motivationwhen engaged in a task that occurs in the presenceof another individual. Without experimental con-trols, it is unclear whether the onlooker who laterapproaches and interacts with the object in ques

tion copied the model’s action, or instead learnedto produce the same behavior by individual trial-and-error learning. Observers may also learn aboutthe causal structure of actions by observing amodel. For example, an individual who watches amodel use a rake to reach a food item may learnthat the rake may be used to attain out-of-reachfood, but not that there is a specific technique forusing rakes. This mode of social learning, wheresubjects learn the causal relationship between anobject (e.g., a tool) and a desired outcome (e.g.,food), has been described as the “emulation ofaffordances” or emulation learning (4). However,Whiten and Ham (5) have argued that individualsin these studies may be copying the goals of themodel (not necessarily their specific techniques).As a result, these authors prefer to call this mech-anism “goal emulation.”

13. Both Horatio and Oberon each served as a “student”and as an “expert.” Experts were trained in isolation(with the partition dividing the two chambers) untilthey completed at least 65% of the trials correctlyduring two consecutive sessions.

14. A. Whiten, J. Comp. Psychol. 112, 270 (1998).15. A. Whiten, D. M. Custance, J. C. Gomez, P. Teixidor,

K. A. Bard, J. Comp. Psychol. 110, 3 (1996).16. M. Tomasello, E. S. Savage-Rumbaugh, A. C. Kruger,

Child Dev. 64, 1688 (1993).17. K. Nagell, R. Olguin, M. Tomasello, J. Comp. Psychol.

107, 174 (1993).18. R. Byrne, A. Russon, Behav. Brain Sci. 21, 667 (1998).19. C. Heyes, Trends Cognit. Sci. 5, 253 (2001).20. M. Tomasello, M. Davis-Dasilva, L. Camak, K. Bard,

Hum. Evol. 2, 175 (1987).21. E. Visalberghi, D. Fragaszy, in “Language” and Intelli-

gence in Monkeys and Apes, S. Parker, K. Gibson, Eds.(Cambridge Univ. Press, Cambridge, 1990), pp. 247–273.

22. E. Visalberghi, M. Tomasello, Behav. Process. 42, 189(1998).

23. M. Hauser, in Machiavellian Intelligence, R. Byrne, A.Whiten, Eds. (Oxford Univ. Press, Oxford, 1988), pp.327–343.

24. M. Tomasello, in “Language” and Intelligence in Mon-keys and Apes, S. Parker, K. Gibson, Eds. (CambridgeUniv. Press, Cambridge, 1990), pp. 274–311.

25. A. Whiten, in The Imitative Mind: Development, Evo-lution, and Brain Bases, A. Meltzoff, W. Prinz, Eds.(Cambridge Univ. Press, Cambridge, 2002), pp. 98–121.

26. R. Byrne, in The Imitative Mind: Development, Evolu-tion, and Brain Bases, A. Meltzoff, W. Prinz, Eds.(Cambridge Univ. Press, Cambridge, 2002), pp. 123–140.

27. G. Gergely, H. Bekkering, I. Kiraly, Nature 415, 755(2002).

28. G. Rizzolatti, L. Fadiga, Novartis Found. Symp. 218, 81(1998).

29. T. Jellema, C. Baker, B. Wicker, D. Perrett, Brain Cogn.44, 280 (2000).

30. We thank all the members of the Primate CognitionLab for their assistance. Supported by National Insti-tute of Mental Health grant R01 MH40462 (H.S.T.).

Supporting Online Materialwww.sciencemag.org/cgi/content/full/305/5682/407/DC1Materials and MethodsFigs. S1 to S3Tables S1 and S2Movie S1References

14 April 2004; accepted 21 June 2004

R E P O R T S

16 JULY 2004 VOL 305 SCIENCE www.sciencemag.org410