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Brain and Cognition 57 (2005) 264–275

Spatial awareness, alertness, and ADHD: The re-emergenceof unilateral neglect with time-on-task

Melanie Georgea,b, Veronika Doblerc, Elaine Nichollsd, Tom Manlya,*

a MRC Cognition and Brain Sciences Unit, Cambridge, United Kingdomb Royal Holloway, University of London, London, United Kingdom

c Department of Experimental Psychology, University of Cambridge, Cambridge, United Kingdomd MRC-ESS in Children�s Middle Ear Disease, Cambridge, United Kingdom

Accepted 16 September 2004Available online 5 November 2004

Abstract

Studies examining a relationship between attention deficit hyperactivity disorder (ADHD) and relative visual inattention towardsleft space have produced inconsistent results. Here, based on previous studies with adult neurological patients who show very severeinattention to the left, we examine whether any spatial bias in ADHD may be modulated by changes in alertness levels. In a singlecase, we found that inattention to the left—that was intermittently apparent—dramatically increased as a function of time-on-task.No significant changes were observed on the right. The implications for clinical assessment and research design are discussed.� 2004 Elsevier Inc. All rights reserved.

Keywords: Spatial neglect; Attention deficit hyperactivity disorder; Arousal

1. Introduction

A number of studies have shown an association be-tween a diagnosis of childhood attention deficit hyperac-tivity disorder (ADHD) and a relative reduction inawareness for visual information presented in left space(Carter, Krener, Chaderjian, Northcutt, & Wolfe, 1995;Nigg, Swanson, & Hinshaw, 1997; Sheppard, Bradshaw,Mattingley, & Lee, 1999; Voeller & Heilman, 1988). Atleast two studies have, however, found no such relation-ship (BenArtsy, Glicksohn, Soroker, Margalit, &Myslobodsky, 1996; Klimkeit, Mattingley, Sheppard,Lee, & Bradshaw, 2003). These divergent findings mayresult from, for example, differences in measure sensitiv-ity and selection criteria. In addition, it is possible thatthe phenomenon of leftward inattention is itself inher-ently variable—present at some times, absent at others.

0278-2626/$ - see front matter � 2004 Elsevier Inc. All rights reserved.

doi:10.1016/j.bandc.2004.09.003

* Corresponding author. Fax +44 1223 516630.E-mail address: [email protected] (T. Manly).

Such variability would have obvious implications forclinical assessment and the design of research studiesthat examine prevalence. In addition, if we are able toidentify factors that reliably modulate its expression, itoffers potential insights into why some children showthis spatial problem at all, and how it might be bestmanaged.

At the outset of this introduction, we first turn to per-tinent adult neuropsychological literature, in particularthe links between strong spatial biases in attention, righthemisphere damage and co-existing deficits in alertness/sustained attention. We then explore existing studiessuggesting that this relationship may also be present inchildren diagnosed with ADHD. For both adults andchildren, modulation of spatial bias with changes inarousal forms a better test of a functional relationshipthan simple association. Accordingly, we examinewhether the spatial bias intermittently shown by onechild with ADHD can be exacerbated by reductions inarousal levels.

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M. George et al. / Brain and Cognition 57 (2005) 264–275 265

1.1. Spatial inattention in adults and links to alertness/

sustained attention

The vulnerability of our capacity to allocate attentionto both sides of space is evidenced by the frequency ofpathological spatial biases following unilateral strokein adulthood. Up to 82% of patients with right hemi-sphere damage, if tested within a few days of the stroke,will ignore information from the left side of space tosome degree. Similarly, about 65% of patients with lefthemisphere damage will show the opposite bias (Stone,Halligan, & Greenwood, 1993). Such biases have beenobserved following damage to a wide variety of brain re-gions including the parietal, temporal, and frontal lobesand to subcortical structures (Karnath, Ferber, & Him-melbach, 2001; Mort et al., 2003). Because neglect canoccur within or across different modalities (Mattingley,Driver, Beschin, & Robertson, 1997), is dissociable frombasic sensory loss (Walker, Findlay, Young, & Welch,1991), and can vary in its severity depending on factorssuch as arousal or concurrent attentional demands (Bar-tolomeo, 2000; Robertson, Mattingley, Rorden, & Ror-den, 1998)—it is generally considered to be an‘‘attentional’’ phenomenon. Clinically, it is associatedwith slowed recovery, difficulties in many activities ofdaily life, and a high degree of dependence on others(Paolucci, Antonucci, Grasso, & Pizzamiglio, 2001).

Although, as discussed, spatial neglect occurs follow-ing right and left hemisphere lesions, there is a strikingdisparity in the distribution of the disorder once the ini-tial post-stroke period has passed. Almost all patientswith chronic manifestations have right hemisphere le-sions and neglect left space (e.g., Stone et al., 1991).One account of this asymmetric recovery pattern is thatdamage to other right hemisphere dominated functionsmay impede what is otherwise a fairly rapid adjustmentthat re-establishes balance within the system (Heilman &Van Den Abell, 1978; Posner, 1993; Robertson, Manly,Beschin et al., 1997; Robertson, Mattingley, Rorden, &Driver, 1998). The prime suspect in this respect is afronto-parietal, right hemisphere dominant system in-volved in maintaining a alert, attentive state (e.g., Lewinet al., 1996; Pardo, Fox, & Raichle, 1991; Rueckert &Grafman, 1996; Sturm et al., 1999; Wilkins, Shallice,& McCarthy, 1987). Notably, this network closely over-laps regions implicated in the aetiology of spatialneglect.

Clinical observations that chronic neglect patients of-ten appear drowsy and to have difficulty in remainingengaged in even non-spatial tasks has received experi-mental support (Robertson, Manly, Beschin et al.,1997; Samuelsson, Hjelmquist, Jensen, Ekholm, &Blomstrand, 1998). Stronger evidence of a functional

relationship between these two capacities comes fromthe observations that neglect can be temporarily reducedafter exposure to alerting tones (Robertson, Mattingley,

Rorden, & Driver, 1998) or medication (Hurford, Strin-ger, & Jann, 1998), and can be exacerbated by sedatives(Lazar et al., 2002).

Such findings raise the question of whether states oflowered alertness simply serve to worsen or prolong aco-existing spatial deficit or whether, due to the inter-connections of these systems, reductions in arousalmay be sufficient to induce a spatial bias away fromthe left. If this is the case, it is then of clinical and theo-retical interest to ask whether other groups, primarilydefined by impairments in non-spatial attention andlow alertness, may also be vulnerable to a bias in atten-tion away from the left. Children diagnosed with atten-tion deficit hyperactivity disorder may form one suchgroup.

1.2. Attention deficit hyperactivity disorder—a deficit in

alertness?

ADHD is said to be present if children show at least 6of 18 difficulties listed within two dimensions (inatten-tion and hyperactivity–impuslivity) of the Diagnosticand Statistical Manual of the American PsychiatricAssociation (1994). There are currently no clear biolog-ical markers and no overwhelming consensus on aetiol-ogy or underlying brain abnormality. The disorder has astrong heritability index however, and genetic studiessuggest that the disorder may be better considered asan extreme on a continuum rather than as a distinct en-tity (Levy, Hay, McStephen, Wood, & Waldman, 1997).In terms of the nature of this continuum, there are sug-gestions that the right hemisphere may play a role. Low-ered right hemisphere activity, particularly in rightfrontal regions, has been reported (Casey et al., 1996;Castellanos et al., 1996; Lou, Henriksen, Bruhn, Borner,& Nielsen, 1989; Rubia et al., 1999). Disruptions to neu-rotransmitter systems such as noradrenaline, stronglyinnervated within prefrontal regions, have also beenimplicated (Karstaedt et al., 1994; Solanto, 2002; Stark-stein, Moran, Bowersox, & Robinson, 1988). Given theassociation of these regions with sustained attention/alertness in adults, it might be expected that capacityin this respect—as suggested in the diagnostic crite-ria—may be reduced.

Variations in selection criteria, age and the presenceof co-morbidity can make comparison across differentADHD studies difficult. In the case of sustained atten-tion some, but not all, psychometric studies have re-ported relative deficits (e.g., Barkley, Grodzinsky, &DuPaul, 1992; Chee, Logan, Schachar, Lindsay, &Wachsmith, 1989; Grodzinsky & Diamond, 1992; Har-per & Ottinger, 1992; Hooks, Milich, & Lorch, 1994).On the face of it, the idea that these often excitableand energetic children suffer from lowered states ofalertness seems rather less plausible. However, muchas many parents know that their children can become

266 M. George et al. / Brain and Cognition 57 (2005) 264–275

energetically ‘‘over-tired’’, influential views of ADHDsuggest that hyperactivity may serve as behaviouralcompensation for chronically lowered levels of alertness(e.g., Antrop, Roeyers, Van Oost, & Buysee, 2000).There is certainly evidence, for example, that ADHDchildren fall asleep more quickly than age matched con-trol groups when deprived of external stimulation(Brown & Modestino, 2000). Perhaps the most compel-ling and replicated finding in this respect, however, liesin the �paradoxical� calming effects of stimulant medica-tion such as methylphenidate (Ritalin). Interestingly,there is evidence that chronically lowered activation inthe right prefrontal cortex discussed above may be nor-malised by methylphenidate (Castellanos & Tannock,2002; Lou et al., 1989; Vaidya, Austin, Kikkorian,Ridlehuber, & Glover, 1998).

There is clearly a danger in extrapolating from the ef-fects of brain damage in maturity as a means of under-standing developmental difficulties. However, there are,as discussed, good reasons to believe that some childrenwith the ADHD diagnosis have sustained attention/arousal deficits that are similar to those seen followingpredominantly right hemisphere lesions in adulthood.The question here is whether these are accompaniedby a higher risk of spatial bias—specifically, away fromthe left.

1.3. Studies of spatial attention in children with ADHD

Voeller and Heilman (1988) administered a clinicaltest of neglect (a cancellation task in which the partici-pants were asked to cross out all, or a subset of, stimulidistributed over a page) to a group of boys with theADHD diagnosis. They reported a disproportionatenumber of left-sided target omissions in the clinicalgroup—as well as noting a number of subtle left-sidedneurological signs, and raised the question of whetherADHD may be a neglect syndrome. This suggestionwas supported by at least three subsequent studies. Nigget al. (1997) assessed boys with the ADHD diagnosis ona speeded computerised test and reported slowed re-sponses specific to left sided stimuli (a trend that wasalso apparent in their parents). Sheppard et al. (1999)asked children to estimate the centre point of horizontallines and found that the bisections of children withADHD were modestly but significantly to the right ofthose of a control group—suggesting that the leftwardextent of the line has been relatively ignored. This pat-tern disappeared when the ADHD group resumed meth-ylphenidate medication. Carter et al. (1995) reportedreaction time performance on a covert attentional cue-ing paradigm in a group of 20 children with ADHD thatwas, relative to controls, suggestive of right hemisphereinefficiency.

Manly, Robertson, and Verity (1997) described a 9-year-old boy with ADHD who showed a pattern of inat-

tention to the left across a number of tests. This bias wasquite as severe as that seen in many adult stroke pa-tients. This extraordinary neglect was apparent despitean entirely unremarkable medical history, an aboveaverage IQ, and a completely normal MRI scan. Dobler,Manly, Verity, Woolrych, and Robertson (2003) re-cently described a very similar boy who, again, per-formed well on verbal tasks, who had no basic visualdifficulty, no obvious brain abnormality but yet whoagain consistently missed a substantial proportion ofinformation presented to the left side of a page or com-puter screen and who met DSM-IV criteria for ADHD.Replicating Robertson, Mattingley, Rorden et al.�s(1998) work with adult neglect patients and echoingthe results of Sheppard et al. (1999) with stimulant med-ication, they reported a significant reduction in theseverity of neglect when the boy was exposed to rela-tively loud, alerting tones immediately before makinga spatial judgement.

In contrast to the above studies, BenArtsy et al.(1996) were unable to find any compelling evidence ofa lateralised attentional bias in a group of 20 boys withADHD on either a cancellation or line bisection test. Aninteresting aspect of this study was that, to disambiguateany effect of ADHD from the possible effects of mildbrain dysfunction, children with �soft neurological signs�of right hemisphere difficulties (e.g., left limb clumsiness)were excluded. Clearly this approach is somewhat atodds with the view that ADHD may primarily reflecta developmental dysfunction of the right hemisphere.It nevertheless raises an interesting question as towhether other evidence of lateralised difficulty may benecessary for, or at least strongly associated with, a spa-tial bias in such children. Recently however, Klimkeit etal. (2003), who did not use these exclusion criteria, sim-ilarly found little evidence for a lateralised bias among17 ADHD children. The children were asked to performtwo potentially very sensitive tasks (judging chimericfaces—see Mattingley, Bradshaw, Phillips, & Bradshaw,1993) and the greyscales task—see Mattingley, Brad-shaw, Bradshaw, and Nettleton (1994) that did not re-quire a motor response. On this basis, the authorsspeculated that a motor response may be necessary toobserve spatial biases in ADHD. Recent evidence Do-bler et al. (in press), using paradigms that do not requireeye movements or manual responses, suggests that thismay not be the case. In accounting for the variabilityin findings, it is possible to argue that ADHD mightbe associated with a mild increased risk of spatial biasaway from the left. Whether or not group effects are sig-nificant will therefore depend on group size and luck.Alternatively, it is possible that children who show arightward spatial bias (possibly as a result of right hemi-sphere dysfunction or immaturity) are likely—in addi-tion—to show a pattern of non-spatial attentionaldeficits that may bring them within the ADHD criteria.


Again, whether or not a group study would reveal a sig-nificant effect would depend, as suggested by BenArtsyet al. (1996) on the proportion of such children in thesample. A third issue—and one that we address here—is whether variability in testing conditions might ac-count for some variability in findings.

1.4. The aims of the current study

The severity of neglect shown by a brain injured adultis often rather variable, changing between one task andanother and within the same task at different times. Suchmodulation has been a key to experimental investiga-tions of the disorder and has formed the basis of a num-ber of rehabilitation strategies (Robertson, Mattingley,Rorden, & Driver, 1998; Robertson & North, 1992).By extension, we might expect the spatial biases of chil-dren to be influenced by many factors such as the pres-ence of strongly competitive visual input from the right,being engaged in secondary tasks and so forth. Giventhe relationship between arousal and neglect in adults,it also seems reasonable to suggest that the severity ofany spatial bias may be influenced by the child�s stateof alertness at the time of assessment—in addition toany more chronic or stable difficulties in this respect.This is already indicated, to a degree, by the findingsof Sheppard et al. (1999) and Dobler et al. (2003) whoreduced the spatial bias shown by children with ADHDusing stimulating sounds or medication. The questionwe address here is whether we can go in the oppositedirection. Can we, by boring repetition of the same task,temporarily exacerbate a spatial bias?

2. Case study

2.1. Background

DA was an eight year and six-month-old boy. Hecame to our attention as part of a larger study examin-ing spatial attention function in children who find sus-tained attention tests difficult. DA�s parents attended alocal ADHD support group and volunteered to assistin the research after seeing an article we had writtenfor the groups� newsletter. The following case studywas conducted with informed parental consent and theapproval of the Local Research Ethics Committee.

DA was of normal birth and reached developmentalmilestones appropriately. He had never been hospita-lised or suffered from a serious illness. His mother re-ported that he did have a ‘‘bang to the head’’ ataround the age of 3–4 years, although it appears thatthis did not result in a loss of consciousness nor wasany further treatment considered necessary by his gen-eral practitioner. No one in DA�s immediate familyhas been diagnosed with ADHD or has suffered from

developmental problems. A cousin was, however, re-ported to have been referred for assessment for possibleADHD. Other than his problems with attention andhyperactivity, and a degree of clumsiness, he was consid-ered a healthy boy. Certainly neither his parents orteachers had noted any particular spatial problems. Heis right handed and does not require glasses.

From DA�s mother�s report it appears that, from anearly age, he exhibited considerable hyperactivity to apoint that was disruptive to those around him and hisown educational opportunities. He was referred for spe-cialist assessment to the Developmental PsychiatryTeam at his local Family and Child Centre. He was gi-ven the diagnosis of ADHD according to DSM-IV crite-ria and was prescribed methylphenidate medication. Inaddition, due to the disruptive effects of his behaviourat school, he was given a Statement of Special Educa-tional Needs (a formal aspect of the UK education sys-tem that entitles children to special provision) andreceived additional support whilst attending mainstreamschool.

2.1.1. General cognitive abilities and ratings of behaviour

DA was seen for the initial session at his school. Test-ing took place in a quiet room that was relatively freefrom distractions. In common with all of the childrenin the larger study, DA�s parents were asked not to givehim his standard methylphenidate medication on themorning of this first assessment. Ritalin has a peak clin-ical effect 1–2h after administration, with the main ef-fects lasting between 2 and 5h (Wilens, Spencer, &Biederman, 2000). With his previous dose having beengiven some 21h before, DA would therefore have beenrelatively free from the effects of this drug during thisfirst testing session. As part of his initial assessment,DA was administered the Wechsler Abbreviated Scaleof Intelligence. As shown in Table 1, his performancewas slightly above average on the verbal subtests andat an average level for the performance subtests. Thissuggests that any problems in sustained attention or vi-sual attention are not part of a generalised intellectualdisability.

DA�s parents and his teacher were also asked to com-plete the Strengths and Difficulties Questionnaire(Goodman, 1999). This is a 25 item measure that asksparents/teachers to select one of 3 responses to state-ments about the child (‘‘not true’’, ‘‘somewhat true’’ or‘‘certainly true’’). The items cover emotional problems(e.g., ‘‘often unhappy, down-hearted or tearful’’), con-duct problems (e.g., ‘‘steals from home, school or else-where’’), hyperactivity (e.g., ‘‘constantly fidgeting orsquirmy’’), peer problems (e.g., ‘‘rather solitary, tendsto play alone’’), and pro-social behaviour (e.g., ‘‘consid-erate of other people�s feelings’’). All but the last cate-gory contribute to an overall score. As can be seen inTable 1, DA�s parental ratings were abnormally high

Table 1Summary of DA�s scores on the Wechsler Abbreviated Scale ofIntelligence and the ratings of his parent and teacher on the strengthsand difficulties questionnaire

Subtests T Score IQ

Wechsler Abbreviated Scale of Intelligence

Vocabulary 56Similarities 52Block design 47Matrix reasoning 53Estimated verbal IQ 108Estimated performance IQ 100

Area Parent Teacher

Strength and difficulties questionnaires

Emotional symptom 8—Abnormal 5—BorderlineConduct problems 6—Abnormal 5—AbnormalHyperactivity 8—Abnormal 10—AbnormalPeer problems 7—Abnormal 7—AbnormalTotal of difficulties scales 29—Abnormal 27—AbnormalPro-social behaviour 4—Abnormal 3—Abnormal


on all of the categories when compared with the pub-lished norms. His teacher�s ratings were consistent withthis pattern, the slight exception being emotional prob-lems. Here, the teacher�s ratings were at a borderline le-vel. In line with aspects of these reports, DA appeared tovery rapidly lose interest in tasks, would get up and walkaround the room and explain that he found the testsboring. However, with suitable encouragement he couldusually complete the tasks he was given and in somecases, in particular the subtests of the WASI, performrather well.

2.2. Initial assessment of sustained and spatial attention

2.2.1. Sustained attention

DA was administered two tests of sustained attentionfrom the Test of Everyday Attention for Children Bat-tery (TEA-Ch; Manly et al., 2001; Manly, Robertson,Anderson, & Nimmo-Smith, 1999)

2.2.1.1. Score!. In the first, Score! children are asked tolisten to a tape player and to count the number of iden-tical sounds that are played within each item of the test(as if they are keeping score by listening to the winningsounds in a computer game). In each item, between 9and 15 sounds are presented, the silent intervals betweenthe sounds varying between 0.5 and 5s. The child�s abil-ity to count to 15 and his or her comprehension of thetest are initially assessed using practice items. Ten testitems are then administered. It has been argued thatthe sustained attention demands of the test come frombridging the long and unpredictable intervals and in‘‘keeping one�s mind’’ on this tedious task—rather thanthe numerocity demands per se. There is certainly agood degree of convergence from adult neuropsychol-ogy and functional imaging literature that performance

on this measure is reliant on regions, including in theright prefrontal cortex, that have been ascribed to sus-tained attention (Lewin et al., 1996; Pardo et al., 1991;Wilkins et al., 1987). This is also an adapted form ofthe tone-counting sustained attention measure thatwas significantly associated with chronic neglect in anadult right hemisphere sample (Robertson, Manly, Bes-chin et al., 1997).

Although he was able to get through the practiceitems, DA was unable to give the correct total for anyof the 10 test items. DA certainly gave the impressionthat he was trying to perform well on the test, for exam-ple by sitting still, not speaking during the test items andproviding an answer at the end of each item. Notably allhis answers were lower than the actual number of tonespresented and offered as if they were correct. Thissuggests that his poor performance was due to lapsingattention rather than poor motivation, compliance, orcomprehension—and that he was not simply guessing.His score fell below the first percentile for boys of his age.

2.2.1.2. Walk Don�t Walk. The second sustained atten-tion measure was the Walk Don�t Walk subtest—de-rived from the adult sustained attention to responsetest (SART; Robertson, Manly, Andrade, Baddeley, &Yiend, 1997). In this subtest, children are given a29.0cm · 20.3cm stimulus sheet showing 22 paths, eachmade up of 14 square steps. They are asked to listen to asequence of regular tones presented using a tape playerand, following each tone to �take a step� down one ofthe paths by dotting each square in turn with a markerpen. In each trial, one tone in the sequence ends unpre-dictably in a cartoon exclamation (‘‘D�oh!’’), indicatingthat the next step should not be taken. Following twopractice trials, 20 test trials are administered, the finalscore being the number of trials where children success-fully withhold their responses after the �no-go� tone. Therationale, as with the SART, is that children must ac-tively maintain attention over their own responses andresist lapsing into a rather automatic, stimulus-drivenmode of responding if they are to avoid errors. DAunderstood the task and was able to successfully com-plete 5 of the 20 items. This level of performance was,however, below the 5th percentile for children of his age.

2.2.2. Spatial attentionOne difficulty in assessing spatial attention in children

lies in the lack of normed, standardised measures for thispopulation. Although this leaves a question mark overwhether a performance is strictly ‘‘impaired’’, wherepossible we will discuss DA�s results with reference toour own data from this and other studies.

2.2.2.1. Star Cancellation. The standard Star Cancella-tion test (Wilson, Cockburn, & Halligan, 1987) consistsof a white 29.0cm · 20.3cm (landscape orientation)

Fig. 1. Top: Model picture. Bottom: DA�s copy.


sheet showing 56 black small star targets (8mm · 8mm)together with 72 black distractors (larger stars, lettersand words) in a quasi-random distribution (see Fig. 2).At the outset of the test, the examiner places the sheetin front of—and at the midline of—the participant andasks him or her to find and cross out all of the small starson the page. Two stars in the centre of the page are thencrossed out by the examiner to illustrate the procedure.The task has no time limit, participants being asked toindicate when they have completed the task to their sat-isfaction. No restrictions are placed on eye or headmovements. Movement of the sheet or excessive leaningto one side or the other are discouraged by the examiner.Healthy adults almost invariably detect all or the vastmajority of the targets. As part of another study in prep-aration, 126 normal school age boys (mean age 9 years 1month, SD 1 year 5 months) completed this measure andmarked a mean of 26.09/27 targets on the left (SD 2.34)and 25.79/27 (SD 2.70) targets on the right.

DA completed the test and detected 21 targets on theleft and 25 on the right—a performance below the 5thpercentile on the left (when compared with this slightlyolder non-clinical boy population) and at approximatelythe 20th percentile on the right. The results were there-fore suggestive of general inattention and raise the pos-sibility that DA has more difficulty in detecting targetson the left—although were certainly not conclusive inthat respect.

2.2.2.2. Line bisection. Line bisection can form a simpleand sensitive measure of spatial neglect in adults (e.g.,Wilson et al., 1987). In the task, participants are pre-sented with a horizontal line and asked to estimate andmark its centre point. Patients with unilateral neglecttypically mark the line some distance to the right of theobjective centre as if they have failed to take full accountof its leftward extent. In this version of the test, DA wassequentially presented with 10 29.0cm · 20.3cm whitesheets, each showing a 200mm · 1mm horizontal blackline. The 126 boys described above who had completedthe Star Cancellation test also completed a version of thistest. The mean deviation from objective centre in theircase was 5.9mm to the left (SD 5.4). This leftward devi-ation is consistent with previous findings in healthyadults and children and has been interpreted in termsof a normal slight leftward bias in visual attention (Brad-shaw, Nathan, Nettleton, Wilson, & Pierson, 1987).

Nine of DA�s bisections were to the right of objectivecentre (4, 40, 9, 5, 4, 5, 10, 12, 10mm, respectively). Onewas 5mm to the left. Overall his performance was anaverage of 9.4mm to the right (SD 11.8)—that is,approximately 3 standard deviations from the meanfor 126 boys from the non-clinical population.

2.2.2.3. Drawing. Copying and drawing tasks are quitecommonly used in the assessment of adult unilateral ne-

glect—although given the wide variety in people�s skillsin this respect, can be difficult to interpret. We asked DAto copy a simple scene showing a house, two trees andthe sun. As can be see in Fig. 1, his copy was ratherpoor. In particular, he omitted the chimney from the lefthand side of the house and curiously extended the leftsection of the house.

2.2.2.4. Visual and tactile extinction. To examine visualextinction we used a conventional bedside confrontationtest. The examiner sat facing DA such that her face wasapproximately 40cm away from—and on a level with—his face. At eye level, the examiner� hands were posi-tioned symmetrically with respect to her face, the totaldistance between the hands being approximately80 cm. In each trial, DA was first asked to look at theexaminer�s nose and then to report whether she hadmoved the index finger of her left hand, her right hand,of both hands or of neither hand. Movements were a ra-pid bending of the tip of the index finger by approxi-mately 1cm. Forty trials were administered in a pre-setrandom sequence comprising 8 left only, 8 right only,14 both hand simultaneous, and 10 neither hand trials.Extinction is said to occur when a lateralised stimuluscan be detected in isolation but not when presented atthe same time as a competing stimulus in the oppositefield.

DA was able to correctly identify all of the left-only,right-only and no-movement trials. He correctly identi-fied 13 of the 14 bilateral simultaneous trials. On theincorrect trial he reported seeing no movements. Thisis not the usual pattern for extinction where, for righthemisphere patients, the typical pattern would be to re-port a bilateral trial as being only on the right. Thisrather crude assessment whilst suggestive of occasionalinattention or distraction, does not therefore offer anygood evidence of attentional extinction.

The tactile extinction test was as described for visualextinction above with the exception that DA was askedto close his eyes and report whether he had received a

Fig. 2. One of DA�s performances on the Star Cancellation subtest. Targets are small stars, DA�s omissions highlighted.


light touch on the back of his left hand, right hand, bothhands or neither hand. The touches were delivered usingsetting 2 on the stimulus delivery Neurometers from theRivermead Assessment of Somatosensory Performance(RASP: Winward, Halligan, & Wade, 2000). The Neu-rometers use a spring to standardise the pressure oftouch on the skin, a setting of 2 corresponding to67.5g. Because the action of the Neurometers producesa quiet click, both were depressed in each trial, either onthe back of DA�s hand to deliver a stimulus or on theexaminer�s knee to produce the equivalent sound. Thir-teen single left and single right trials were administered,interspersed with 19 both hand, and 15 no-touch, trials.On all trials, DA�s hands were resting equidistant to hismidline on a table in front of him.

DA correctly identified all of the right-only trials, thebilateral trials and the no-touch trials. For 3 of the 13left-only trials he reported that he did not know wherehe had been touched (it was permissible to indicate wherehe had been touched by indicating the hand rather thanusing the verbal label left or right). Again, the resultsprovide no evidence of tactile extinction. The pattern ishowever consistent with some uncertainty about thelocation of single left touches—not sufficient to supporta full report of having been on the right (a phenomenonknown as allochiria) but sufficient to induce doubt aboutit having been on the left. An alternative account is thatthe three touches to the left happened to coincide withperiods of inattention/distraction.

In summary, although none of the measures so fardescribed provide unambiguous evidence of a develop-mental neglect of left space, the convergence across thecancellation test, line bisection and drawing tasks (andpossibly the tactile extinction test) is at least suggestiveof difficulties in this respect. Our confidence that thesewere true positive results was however weakened byDA�s performance of the tasks at subsequent sessions.

2.3. Subsequent assessment of spatial function

DA was seen briefly approximately 3 weeks after theinitial session. Unfortunately, due to some confusionover the date of the appointment at school, he had beengiven his morning dose of methylphenidate. He was re-administered the Star Cancellation test. He made noomissions. Due to changes in his school schedule andour own commitments, it was not possible to see DAagain for another 3 months. Then, in another brief ses-sion he performed the Star Cancellation again andmissed 4 targets on the left whilst finding them all onthe right. His parents had not given him methylpheni-date on the morning of this assessment.

The next session took place some 4 months later.Again, DA had been given methylphenidate that morn-ing. On this occasion, he found all of the targets on theStar Cancellation measure. He also showed a modest(normal) leftward deviation on the line bisection test(mean deviation = 4.67 to the left of centre (SD 12.42)and produced a drawing copy that, whilst rather oddlydistributed, nevertheless contained all of the featuresof the original.

Looking at error rates on the cancellation test acrossall of the sessions and separating them into those whereDA had taken methylphenidate and those where he hadnot, there is a statistically significant association be-tween error rates on the left and the presence of thedrug. Here, Fisher�s Z test was used due to the 0 valuein one cell: total leftward omissions off methylpheni-date = 10, total on methylphenidate = 0, Fisher�s Exacttest P = .001). However, these sessions were interspersedwith long and irregular intervals and his methylpheni-date status was not under our experimental control.While methylphenidate has previously been associatedwith reductions in spatial bias away from the left in chil-dren (Sheppard et al., 1999) and adults (Hurford et al.,


1998), we do not have sufficient evidence to claim suchan effect here.

A cautious conclusion at this point would be that DA�sdid not have a specific lateralised bias away from the left,rather his more general attentional problems led him tosometimes make errors on the task that, by chance, weremore frequent on the left. There are however, as dis-cussed, reasonable grounds to predict that (1) if therewas a bias, it would be away from the left and (2) his per-formance on the leftwould be disproportionately affectedby levels of alertness. If it was the case that sometimes wehad seen DA in a relatively alert state and at other timesmore sleepy, bored or distracted, this could account forthe variability in his spatial performance.

To investigate this we addressed the question ofwhether DA�s left neglect might re-emerge over thecourse of a long single session during which he engagedin rather repetitive, unstimulating—even perhaps bor-ing—activity. Long periods spent on a single task tendto reduce electrophysiological correlates of arousal andincrease subjective ratings of, for example, sleepiness.If his current state of arousal was important in influenc-ing his relative awareness of information on the left,would we see significant changes with time-on-task?

2.4. Examining time-on-task effects on the Star

Cancellation measure

2.4.1. Procedure

The Star Cancellation test was administered as previ-ously described. Forty consecutive administrations ofthe task were completed over approximately 45min.

Immediately before, and immediately after, the repeatStar Cancellation procedure, DA was administered theLine Bisection subtest from the Behavioural Inattentiontest. This is a single sheet showing three horizontal lines(each 207-mm long). To avoid participants simply draw-ing a single bisecting mark though all the stimulus lines,

Fig. 3. The pattern of DA omissions over 40 consecut

they are displaced on the horizontal as well as verticalaxis of the sheet. The task is administered as previouslydescribed, with the participant being asked to estimateand mark the centre of each line in turn.

2.4.2. ResultsAlthough difficult to formally quantify, DA

showed—as might be expected—an increase in restless-ness as the repetitive task proceeded and was able tofreely report that the task was losing some of its interest.

2.4.2.1. Star Cancellation. The number of targets omit-ted on each administration of the Star Cancellation taskis shown in Fig. 3. As can be seen in the figure, havingbegun by making no omissions on the first trial, DAthen preceded to make a few omissions on the left andthe right of the sheet over the next few trials—suggestingthat the interpretation of his performance as generallyinattentive rather than spatially biased may be correct.From around trial 7 to trial 20 he makes few omissionswhich are slightly more frequent on the left. After trail20 his variability in detecting targets on the right ofthe sheet almost completely disappears, his detectionrate (with the exception of one omission on trial 31)being at 100%. In contrast, on the left of the sheet he ap-pears to show a substantial increase in the frequency oftrials on which omissions occur and the number of tar-gets omitted on those trials.

We first examined whether time-on-task was signifi-cantly associated with an increase in omissions regard-less of the side on which these occurred (see Table 2).This was the case (Pearson�s v2 = 7.25, P = .007). Toexamine a lateralised effect on this increase in omissionswe fitted a log-linear model to test for the interaction.This yielded two Goodness-of-Fit Test estimatesfor the model (Constant + Correct + Time_period +side + Time_period * Correct + side * Correct + side *Time_period); Likelihood ratio 5.830, df 1, P = .016 and

ive administrations of the Star Cancellation test.

Table 2Results from the repetition of the Star Cancellation measure showing omission levels on the left and right of the sheet during the first and secondhalves of the test session tested against the model of no interaction between side, time-, and omissions

Side Time_period Correct Observed Expected

Count % Count %

1.00 Left 1.00 Early 1.00 Correct 528 24.4 525.540 24.32.00 Incorrect 12 .6 14.460 .7

2.00 Late 1.00 Correct 506 23.4 508.460 23.52.00 Incorrect 34 1.6 31.540 1.5

2.00 Right 1.00 Early 1.00 Correct 536 24.8 538.460 24.92.00 Incorrect 4 .2 1.540 .1

2.00 Late 1.00 Correct 539 25.0 536.540 24.82.00 Incorrect 1 .0 3.460 .2


Pearson v2 6.334, df 1, P = .012. The hypothesis thatomissions would increase disproportionately on the leftof the sheet was therefore supported.

2.4.2.2. Line bisection. Before embarking on the longsession of Star Cancellations, DA bisected lines at amean of 1.3mm to the left of centre (e.g., consistent withthe normal pattern). Following the Star Cancellationshis performance was similar to that at the initialsession—and of adult patients with neglect (mean =30.01mm to the right). Although there is insufficientdata to support statistical analysis, the result is at leastconsistent with a more generalised effect of time-on-taskon spatial performance.

3. Discussion

The results of this case study show that:

1. A boy of normal birth, who performed at an averagelevel on tests of general intellectual function, and inwhom we have no reason to suspect acquired braininjury—performed on spatial tests in a manner simi-lar to that of some adult patients with acquiredlesions to the right hemisphere. As with previousreports (Dobler et al., 2003; Manly et al., 1997) thisdevelopmental unilateral neglect occurred in the con-text of poor performance on sustained attention testsand the ADHD diagnosis.

2. At the initial session, the pattern of inattentiontowards the left was apparent in the Star Cancella-tion, Line bisection and (arguably) drawing-copytasks. In addition to these visuo-motor tasks, his per-formance on a bilateral tactile detection test wassomewhat suggestive of leftward inattention.

3. At a subsequent session there was no evidence of sucha bias. Thereafter, at sessions conducted somemonths apart, poor performance on spatial testswas sometimes present and sometimes absent. Nota-bly, when present, poor performance was always on

the left of the task. There is some suggestion thatDA�s performance may have varied as a function ofwhether or not he had recently taken the stimulantmethylphenidate—although this is not conclusivelyestablished here.

4. Based on the premise that the orientation of spatialattention to the left may be particularly vulnerableto low levels of general alertness we investigatedwhether a ‘‘latent’’ left neglect may re-emerge underrepetitive and un-stimulating conditions. Over 40consecutive presentations of the Star Cancellationmeasure there was a statistically significant increasein omissions between the second and first halves ofthe session. There was also a significant interactionbetween time period and the side of the sheet onwhich omissions occurred—to the detriment of theleft. His performance on a line bisection test con-ducted before and after the Star Cancellation proce-dure suggests that this decline in attention towardsthe left was unlikely to be specific to one task.

In adults, as discussed, persistent spatial neglect isdisproportionately associated with lesions to the righthemisphere and almost invariably affects left space.Within adult right-hemisphere damaged groups, persis-tence of neglect is associated with co-occurring deficitson non-spatial sustained attention tasks. Such an associ-ation could arise for a number of reasons. Firstly, it maysimply be a by-product of lesion extent and severity;large lesions are more likely to compromise more thanone right-hemisphere dominant system and to lead tomore chronic difficulties. Secondly, it could be that alow level of alertness is a rather bad thing for cognitivefunction in general and that impairments, including spa-tial function, may be exacerbated or more likely to per-sist. Thirdly, there could be a rather more intimaterelationship between right hemisphere mechanismsmediating sustained attention/alertness and the capacityto orient attention to the left. Association is a weak toolfor arbitrating between these accounts in comparisonwith experimental modulation. In this respect, the obser-


vation that neglect can be reduced by alerting stimuli(Robertson, Mattingley, Rorden, & Driver, 1998) ormedication (Hurford et al., 1998), and exacerbated bysedation (Lazar et al., 2002) or distraction (Bartolomeo,2000) are potentially more informative.

The situation with regard to an association betweenADHDand leftward inattention is rather similar. ADHDhas a genetic component and has a high degree of co-mor-bidity with other behavioural and learning problems. Onemight, therefore, expect a good number of cognitive/per-ceptual or motor skills to be moderately worse at a grouplevel in comparison with non-ADHD samples—depend-ing upon which exclusion criteria are employed. If as anumber of authors now suggest, ADHDmay have a basisin right hemisphere dysfunction, one might expect left-ward inattention and poor sustained attention again,without a necessary link other than anatomical associa-tion. The results from group studies in this respect havebeen, as discussed, mixed. A positive association wasreported by Carter et al. (1995), Nigg et al. (1997), Shepp-ard et al. (1999) and Voeller and Heilman (1988)—eachstudy reporting inattention to the left. Negative findingshave been reported by BenArtsy et al. (1996) and recentlyby Klimkeit et al. (2003).

The results of this and two previous single case stud-ies are suggestive but cannot, of course, address the issueof a general association between leftward inattentionand ADHD. The relevance of this and a previous casereport (Dobler et al., 2003), the ADHD group studyof Sheppard et al. (1999) and the work with childrenfrom the normal populations reported by Dobler et al.(in press), lie in the observed modulation of spatial func-tion by interventions related to alertness/sustainedattention. In Dobler et al. (2003), a child with rather se-vere neglect showed considerable improvements follow-ing the presentation of alerting loud tones that offeredno specifically spatial information. Sheppard et al.(1999) found that methylphenidate—a stimulant—wasassociated with reduced bias on the line bisection task.Dobler et al. (in press) reports that children from thenon-clinical population (including those with very goodsustained attention) showed a slight but detectable de-cline in performance on left but not right-presentedstimuli over a long testing session. Here, we have shownthat repetitive and rather dull testing was associatedwith a very robust increase in target omissions on theleft but not the right side of the task.

The results support a general hypothesis based onadult and child studies that low levels of alertness/sus-tained attention can exacerbate a spatial bias and thatthis will predominantly affect left space. The results ofDobler et al. (in press) suggest that it may not even benecessary to argue for an interaction between separatespatial and sustained attention deficits, as—in healthychildren—diminishing levels of alertness appeared suffi-cient to induce a slight rightward shift in visual atten-

tion. One influential view of unilateral neglect suggeststhat, in healthy individuals, the two hemispheres of thebrain exist a rather finely balanced competition, eachpreferring to orient into contralateral space (e.g., Kins-bourne, 1977). Disruption to one hemisphere may there-fore allow the other hemisphere to dominate untilbalance is restored. Such a view may help to accountfor why damage to such a wide variety of cortical andsubcortical structures can induce spatial neglect. Itmay also help to explain why reduced activity in a righthemisphere dominant circuit associated with generalalertness may unbalance the system to the detriment ofattention towards left space.

It is fair to say that the majority of leftward inatten-tion reported in children with ADHD has, to date, beenrelatively mild and of uncertain clinical implication. Wehave, however, previously reported two children inwhich this was not the case. In the first (Manly et al.,1997) the child�s neglect led to reading errors that wereoriginally viewed as a developmental dyslexia withoutan obvious spatial component. The second, (Dobler etal., 2003), the child had very poor drawing skills andclumsiness. Again, until our assessment there was nosuspicion by either his parents or teachers that therewas a spatial dimension to these problems. In adults,spatial neglect is associated with poor recovery, notablyin motor systems (e.g., Paolucci, Antonucci et al., 2001;Paolucci, Grasso et al., 2001). Given that the spatialproblems that we have described in children do not seemobvious to those around them, it is unlikely that we willbe able to address the full clinical implications unlesssensitive spatial assessment is performed in large-scaleresearch or in routine clinical practice. However, the re-sults that we present here suggest that one-off, brief clin-ical administrations of spatial tests—arguably due to theinherently alerting novelty of the task and clinical con-text—may under-represent the potential for spatialproblems in children. If it proves to be a general feature,this factor should be considered in both research designand clinical assessment.

Acknowledgments

This work was supported by the UK Medical Re-search Council. We are grateful to Professor Mark Hag-gard for his useful comments on the manuscript.

References

American Psychiatric Association (1994). Diagnostic and statistical

manual of mental disorders. (4th ed.). Washington DC: AmericanPsychiatric Association.

Antrop, I., Roeyers, H., Van Oost, P., & Buysee, A. (2000).Stimulation seeking and hyperactivity in children with ADHD.Journal of Child Psychology and Psychiatry, 41(2), 225–231.


Barkley, R. A., Grodzinsky, G., & DuPaul, G. J. (1992). Frontal lobefunctions in attention deficit disorder with and without hyperac-tivity: A review and research support. The Clinical Neuropsychol-

ogist, 8, 121–140.Bartolomeo, P. (2000). Inhibitory processes and spatial bias after right

hemisphere damage. Neuropsychological Rehabilitation, 10(5),511–526.

BenArtsy, A., Glicksohn, J., Soroker, N., Margalit, M., & Myslobod-sky, M. (1996). An assessment of hemineglect in children withattention-deficit hyperactivity disorder. Developmental Neuropsy-

chology, 12(3), 271–281.Bradshaw, J. L., Nathan, G., Nettleton, N. C., Wilson, L., & Pierson,

J. (1987). Why is there a left side underestimation in rod bisection.Neuropsychologia, 25, 735–738.

Brown, T. E., & Modestino, E. J. (2000). Attention-deficit disorderswith sleep/arousal disturbances. In T. E. Brown (Ed.), Attention-deficit disorders and comorbidities in children, adolescents, and adults

(pp. 341–362). Washington DC: American Psychiatric Press.Carter, C. S., Krener, P., Chaderjian, M., Northcutt, C., & Wolfe, V.

(1995). Asymmetrical visual–spatial attentional performance inADHD: Evidence for a right hemispheric deficit. Biological

Psychiatry, 37(11), 789–797.Casey, B. J., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L.

E., Cohen, J. D., et al. (1996). A pediatric functional MRI study ofprefrontal activation during performance of a go-no-go task.NeuroImage, 3(2), S593.

Castellanos, F., & Tannock, R. (2002). Neuroscience of attentiondeficit/hyperactivity disorder: The search for endophenotypes.Nature Reviews, 3, 617–628.

Castellanos, F. X., Giedd, J. N., Marsh, W. L., Hamburger, S. D.,Vaituzis, A. C., Dickstein, D. P., et al. (1996). Quantitative brainmagnetic-resonance-imaging in attention-deficit hyperactivity dis-order. Archives of General Psychiatry, 53, 607–616.

Chee, P., Logan, G., Schachar, R., Lindsay, P., & Wachsmith, R.(1989). Effects of event rate and display time on sustained attentionin hyperactive, normal and control children. Journal of Abnormal

Child Psychology, 17(4), 371–391.Dobler, V. B., Manly, T., Anker, S., Gilmore, J., Dezeryu, A. M., &

Atkinson, J. (in press). Asymmetric deterioration of spatialawareness with diminishing levels of alertness in normal childrenand children with ADHA. Journal of Child Psychology and

Psychiatry.Dobler, V. B., Manly, T., Verity, C., Woolrych, J., & Robertson, I. H.

(2003). Modulation of spatial attention in a child with develop-mental unilateral neglect. Developmental Medicine and Child

Neurology, 45(4), 282–288.Goodman, R. (1999). The extended version of the strengths and

difficulties questionnaire as a guide to child psychiatric casenessand consequent burden. Journal of Child Psychology and Psychi-

atry, 40, 791–801.Grodzinsky, G. M., & Diamond, R. (1992). Frontal lobe functionin in

boys with attention-deficit hyperactivity disorder. Developmental

Neuropsychology, 8(4), 427–445.Harper, G. W., & Ottinger, D. (1992). The performance of hyperactive

and control preschoolers on a new computerised measure of visualvigilance: The preschool vigilance task. Journal of Child Psychologyand Psychiatry, 33, 1365–1372.

Heilman, K., & Van DenAbell, T. (1978). Right hemisphere domi-nance for mediating cerebral activation. Neuropsychologia, 17,315–321.

Hooks, K., Milich, R., & Lorch, E. (1994). Sustained and selectiveattention in boys with attention deficit hyperactivity disorder.Journal of Clinical Child Psychology, 23, 69–77.

Hurford, P., Stringer, A., & Jann, B. (1998). Neuropharmacologictreatment of hemineglect: A case report comparing bromocriptineand methylphenidate. Archives of Physical Medicine and Rehabil-

itation, 79(3), 346–349.

Karnath, H. O., Ferber, S., & Himmelbach, M. (2001). Spatialawareness is a function of the temporal not the posterior parietallobe. Nature, 411, 950–953.

Karstaedt, P., Kerasidis, H., Pincus, J., Meloni, R., Graham, J., &Gale, K. (1994). Unilateral destruction of dopamine pathwaysincreases ipsilateral striatal serotonin turnover in rats. Experimen-

tal Neurology, 126(1), 25–30.Kinsbourne, M. (1977). Hemi-neglect and hemisphere rivalry. In E. A.

Weinstein & R. P. Friedland (Eds.). Advances in neurology (Vol.18, pp. 41–49). New York: Raven.

Klimkeit, E. I., Mattingley, J. B., Sheppard, D. M., Lee, P., &Bradshaw, J. L. (2003). Perceptual asymmetries in normal childrenand children with attention deficit/hyperactivity disorder. Brain andCognition, 52(2), 205–215.

Lazar, R., Fitzsimmons, B., Marshall, R., Berman, M., Bustillo, M.,Young, W., et al. (2002). Reemergence of stroke deficits withmidazolam challenge. Stroke, 33(1), 283–285.

Levy, F., Hay, D. A., McStephen, M., Wood, C., & Waldman, I.(1997). Attention-deficit hyperactivity disorder: A category or acontinuum? Genetic analysis of a large-scale twin study. Journal ofthe American Academy of Child and Adolescent Psychiatry, 36,737–744.

Lewin, J. S., Friedman, L., Wu, D., Miller, D. A., Thompson, L. A.,Klein, S. K., et al. (1996). Cortical localization of human sustainedattention: Detection with functional MR using a visual vigilanceparadigm. Journal of Computer Assisted Tomography, 20(5),695–701.

Lou, H., Henriksen, L., Bruhn, P., Borner, H., & Nielsen, J. (1989).Striatal dysfunction in attention deficit and hyperkinetic disorder.Archives of Neurology, 46(1 JAN), 48–52.

Manly, T., Anderson, V., Nimmo-Smith, I., Turner, A., Watson, P., &Robertson, I. H. (2001). The differential assessment of children�sattention: The test of everyday attention for children (TEA-Ch),normative sample and ADHD performance. Journal of Child

Psychology and Psychiatry, 42, 1065–1081.Manly, T., Robertson, I. H., Anderson, V. A., & Nimmo-Smith, I.

(1999). TEA-Ch – The test of everyday attention for children. BurySt. Edmunds: Thames Valley Test Company.

Manly, T., Robertson, I. H., & Verity, C. (1997). Developmentalunilateral neglect: A single case study. Neurocase, 3(1), 19–29.

Mattingley, J. B., Bradshaw, J. L., Bradshaw, J. A., & Nettleton, N. C.(1994). Residual right attentional bias after apparent recovery fromright hemisphere damage: Implications for a multicomponentmodel of neglect. Journal of Neurology, Neurosurgery and Psychi-

atry, 57, 597–604.Mattingley, J. B., Bradshaw, J. L., Phillips, J. G., & Bradshaw, J. A.

(1993). Reversed perceptual asymmetry for faces in left unilateralneglect. Brain and Cognition, 23, 145–165.

Mattingley, J. B., Driver, J., Beschin, N., & Robertson, I. H. (1997).Attentional competition between modalities: Extinction betweentouch and vision after right hemisphere damage. Neuropsychologia,

35(6), 867–880.Mort, D. J., Malhotra, P., Mannan, S. K., Rorden, C., Pambakian, A.,

Kennard, C., et al. (2003). The anatomy of visual neglect. Brain,126, 1986–1997.

Nigg, J. T., Swanson, J. M., & Hinshaw, S. P. (1997). Covert spatialattention in boys with attention deficit hyperactivity disorder:Lateral effects, methylphenidate response and results for parents.Neuropsychologia, 35(2), 165–176.

Paolucci, S., Antonucci, G., Grasso, M., & Pizzamiglio, L. (2001). Therole of unilateral spatial neglect in rehabilitation of right brain-damaged ischemic stroke patients: A matched comparison.Archives of Physical Medicine and Rehabilitation, 82(6), 743–749.

Paolucci, S., Grasso, M. G., Antonucci, G., Bragoni, M., Troisi, E.,Morelli, D., et al. (2001). Mobility status after inpatient strokerehabilitation: 1-Year follow-up and prognostic factors. Archives ofPhysical Medicine and Rehabilitation, 82(1), 2–8.


Pardo, J. V., Fox, P. T., & Raichle, M. E. (1991). Localization of ahuman system for sustained attention by positron emissiontomography. Nature, 349, 61–64.

Posner, M. I. (1993). Interaction of arousal and selection in theposterior attention network. In A. Baddeley & L. Weiskrantz(Eds.), Attention: Selection, Awareness and Control (pp. 390–405).Oxford: Clarendon Press.

Robertson, I. H., Manly, T., Andrade, J., Baddeley, B. T., & Yiend, J.(1997). �Oops!�: Performance correlates of everyday attentionalfailures in traumatic brain injured and normal subjects. Neuro-

psychologia, 35(6), 747–758.Robertson, I. H., Manly, T., Beschin, N., Haeske-Dewick, H.,

Homberg, V., Jehkonen, M., et al. (1997). Auditory sustainedattention is a marker of unilateral spatial neglect. Neuropsycholo-

gia, 35, 1527–1532.Robertson, I. H., Mattingley, J. B., Rorden, C., & Driver, J. (1998).

Phasic alerting of neglect patients overcomes their spatial deficit invisual awareness. Nature, 395, 169–172.

Robertson, I. H., Mattingley, J., Rorden, C., & Rorden, J. (1998).Phasic alerting of neglect patients overcomes their spatial deficit invisual awareness. Nature, 395, 169–172.

Robertson, I. H., & North, N. (1992). Spatio-motor cueing inunilateral neglect: The role of hemispace, hand and motoractivation. Neuropsychologia, 30, 553–563.

Rubia, K., Overmeyer, S., Taylor, E., Brammer, M, Williams, S.,Simmonds, A., et al. (1999). Hypofrontality in attention deficithyperactivity disorder during higher-order motor control: A studywith functional MRI. American Journal of Psychiatry, 156(6),891–896.

Rueckert, L., & Grafman, J. (1996). Sustained attention deficits inpatients with right frontal lesions. Neuropsychologia, 34(10),953–963.

Samuelsson, H., Hjelmquist, E., Jensen, C., Ekholm, S., & Blom-strand, C. (1998). Nonlateralized attentional deficits: An importantcomponent behind persisting visuospatial neglect?. Journal of

Clinical and Experimental Neuropsychology, 20(1 FEB), 73–88.

Sheppard, D. M., Bradshaw, J. L., Mattingley, J. B., & Lee, P. (1999).Effects of stimulant medication on the lateralisation of linebisection judgements of children with attention deficit hyperactivity

disorder. Journal of Neurology, Neurosurgery and Psychiatry, 66(1),57–63.

Solanto, M. (2002). Dopamine dysfunction in AD/HD: Integratingclinical and basic neuroscience research. Behavioural Brain

Research, 130, 65–71.Starkstein, S., Moran, T., Bowersox, J., & Robinson, R. (1988).

Behavioural abnormalities induced by frontal cortical and nucleusaccumbens lesions. Brain Research, 473, 74–80.

Stone, S. P., Halligan, P. W., & Greenwood, R. J. (1993). Theincidence of neglect phenomena and related disorders in patientswith an acute right or left-hemisphere stroke. Age and Ageing,

22(1), 46–52.Stone, S. P., Wilson, B. A., Wroot, A., Halligan, P. W., Lange, L. S.,

Marshall, J. C., et al. (1991). The assessment of visuo-spatial negletafter acute stroke. Journal of Neurology, Neurosurgery and Psychi-

atry, 54, 345–350.Sturm, W., Simone, A., Krause, B., Specht, K., Hesselmann, V.,

Radermacher, I., et al. (1999). Functional anatomy of intrinsicalertness: Evidence for a fronto-parietal-thalamic-brainstem net-work in the right hemisphere. Neuropychologia, 37, 797–805.

Vaidya, C., Austin, G., Kikkorian, G., Ridlehuber, H., & Glover, D.(1998). Selective deficits of methylphenidate in attention deficithyperactivity disorder: A functional magnetic resonanace study.Proceedings of the National Academy of Sciences of the United

States of America, 95, 14494–14499.Voeller, K. K. S., & Heilman, K. M. (1988). Attention deficit disorder

in children: A neglect syndrome?. Neurology, 38, 806–808.Walker, R., Findlay, J. M., Young, A. W., & Welch, J. (1991).

Disentangling neglect and hemianopia. Nia, 29, 1019–1027.Wilens, T., Spencer, T., & Biederman, J. (2000). Pharmacotherapy of

attention-deficit/hyperactivity disorder. In T. Brown (Ed.), Atten-tion-deficit disorders and comorbidities in children, adolescents, and

adults (pp. 509–535). American Psychiatric Publishing.Wilkins, A. J., Shallice, T., & McCarthy, R. (1987). Frontal lesions and

sustained attention. Neuropsychologia, 25, 359–365.Wilson, B., Cockburn, J., & Halligan, P. (1987). The behavioural

inattention test. Titchfield, Hampshire: Thames Valley.Winward, C. E., Halligan, P. W., & Wade, D. T. (2000). Rivermead

assessment of somatosensory performance. Bury St. Edmunds:Thames Valley Test Company.