Effects of Early Focal Brain Injury on Memory for Visuospatial Patterns:Selective Deficits of Global–Local Processing

Joan StilesUniversity of California, San Diego

Catherine SternBrown University

Mark AppelbaumUniversity of California, San Diego

Ruth NassNew York University Medical Center

Doris Trauner and John HesselinkUniversity of California, San Diego

Selective deficits in visuospatial processing are present early in development among children withperinatal focal brain lesions (PL). Children with right hemisphere PL (RPL) are impaired in configuralprocessing, while children with left hemisphere PL (LPL) are impaired in featural processing. Deficitsassociated with LPL are less pervasive than those observed with RPL, but this difference may reflect thestructure of the tasks used for assessment. Many of the tasks used to date may place greater demands onconfigural processing, thus highlighting this deficit in the RPL group. This study employed a taskdesigned to place comparable demands on configural and featural processing, providing the opportunityto obtain within-task evidence of differential deficit. Sixty-two 5- to 14-year-old children (19 RPL, 19LPL, and 24 matched controls) reproduced from memory a series of hierarchical forms (large formscomposed of small forms). Global- and local-level reproduction accuracy was scored. Controls wereequally accurate on global- and local-level reproduction. Children with RPL were selectively impairedon global accuracy, and children with LPL on local accuracy, thus documenting a double dissociation inglobal–local processing.

Keywords: early brain injury, visuospatial processing, selective deficit, global processing, local processing

A critical aspect of visual pattern processing is the ability bothto identify the parts of the visually presented object or array and tounderstand how the parts combine to form a unified whole. Studiesof infants have documented that this basic spatial processingability is available, in rudimentary form, early in development(Cohen & Cashon, 2001; Cohen, Chaput, & Cashon, 2002). How-ever, a large body of data also shows that developmental change invisuospatial processing continues throughout childhood and into

adolescence (Akshoomoff & Stiles, 1995a, 1995b; Dukette &Stiles, 1996, 2001; Feeney & Stiles, 1996; Newcombe & Hutten-locher, 2000; Prather & Bacon, 1986; Stiles & Stern, 2001; Tada& Stiles, 1996). These data suggest that while the basic neuralsystem that mediates part–whole processing may begin to developvery early, it continues to undergo significant developmentalchange for a protracted period of time.

Such findings have important implications for understandingvisuospatial processing following perinatal brain injury. Evidencefor early commitment of the neural system for visuospatial pro-cessing suggests that perinatal injury should result in permanentdeficits. However, the protracted term of visuospatial developmentmay serve to mitigate the effects of early injury and moderatelong-term deficit. Consistent with this latter account, data from ourprevious studies of visuospatial development in children withperinatal focal brain lesions (PL) document both subtle deficit andcontinuing development (Reilly, Levine, Nass, & Stiles, in press;Stiles, Bates, Thal, Trauner, & Reilly, 1998, 2002; Stiles, Nass,Levine, Moses, & Reilly, in press; Stiles, Paul, & Hesselink, 2006;Stiles, Reilly, Paul, & Moses, 2005). The data suggest that devel-opment following early neural insult is dynamic, incorporating theeffects of initial injury into an ongoing developmental process thatentails both biological specification and the capacity for adaptivechange.

The Neural System for Visuospatial Processing

The neural system most closely associated with the visual pars-ing and integration functions necessary to identify an object or

Joan Stiles, Department of Cognitive Science, University of California,San Diego; Catherine Stern, Department of Psychiatry and Human Behav-ior, School of Medicine, Brown University; Mark Appelbaum, Departmentof Psychology, University of California, San Diego; Ruth Nass, Depart-ment of Neurology, New York University Medical Center; Doris Trauner,Departments of Neurosciences and Pediatrics, School of Medicine, Uni-versity of California, San Diego; and John Hesselink, Department ofRadiology, School of Medicine, University of California, San Diego.

Catherine Stern is now in private practice in New York City and WhitePlains, NY.

This work was supported by National Institute of Child Health andHuman Development Grant R01-HD25077, National Institute of Neuro-logical Disorders and Stroke Grant P50-NS22343, and National Institute ofDeafness and Communicative Disorders Grant P50-DC01289. We thankthe parents and children for their participation in the studies presented inthis article.

Correspondence concerning this article should be addressed to JoanStiles, University of California, San Diego, Department of CognitiveScience, 9500 Gilman Drive, La Jolla, CA 92093-0515. E-mail:stiles@ucsd.edu

Neuropsychology Copyright 2008 by the American Psychological Association2008, Vol. 22, No. 1, 61–73 0894-4105/08/$12.00 DOI: 10.1037/0894-4105.22.1.61

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visual scene is the ventral occipital–temporal (VOT) system, the“what” system (Ungerleider & Mishkin, 1982). The VOT systemprojects bilaterally from primary to secondary visual corticeswithin the occipital lobe and then courses ventrally through asso-ciation regions of the temporal lobe. Evidence from studies ofadult patients with localized brain injury suggests that the VOTsystems within each of the two cerebral hemispheres may playcomplementary roles in visual pattern processing.

In adults, injury to occipital–temporal regions of the right hemi-sphere (RH) or left hemisphere (LH) results in selective disruptionof visual pattern processing. Specifically, LH injury compromisesthe ability to encode the parts of a spatial pattern, while RH injuryimpairs pattern integration (e.g., Delis, Kiefner, & Fridlund, 1988;Lamb, Robertson, & Knight, 1989; Robertson & Lamb, 1991;Robertson, Lamb, & Knight, 1988). Data from a study by Delis,Robertson, and Efron (1986) illustrate this dissociation (see Figure1). Adult stroke patients studied a model hierarchical, “global–local” stimulus (e.g., a large “global” M composed of small “local”Zs). After a delay, they were asked to reproduce the pattern frommemory. As illustrated in the figure, memory for global-levelinformation was compromised in patients with RH injury, whilememory for local-level information was affected in patients withLH injury.

The Development of Visuospatial Processing

Studies of typical children have shown that even young infantscan analyze spatial patterns. Early competence has been demon-strated for rudimentary global and local pattern information (Co-hen & Younger, 1984). Further, lateralized differences in config-ural and featural processing have been documented in the first yearof life (Catherwood, Cramm, & Foster, 2003; Deruelle & deSchonen, 1991, 1995, 1998). However, there is also evidence forsubstantial developmental change in visual pattern processing.Change in the complexity and sophistication of spatial analyticprocessing has been documented across the preschool and school-age period (Akshoomoff & Stiles, 1995a, 1995b; Dukette & Stiles,1996, 2001; Feeney & Stiles, 1996; Stiles & Stern, 2001; Tada &

Stiles, 1996). Prather and Bacon (1986) showed that children canattend to either the parts or whole of a spatial pattern, but perfor-mance is systematically influenced by task and stimulus manipu-lations. Newcombe and Huttenlocher (2000) examined how chil-dren parse a visual array and documented systematic change fromthe preschool through the school-age period in children’s concep-tualization of the visual space. Data from our laboratory havedocumented change in the complexity of visuospatial processing in2- to 12-year-olds. Using a variety of tasks, we have shown thathow children process a visual stimulus is affected by both thecomplexity of the stimulus pattern and the sophistication of theprocessing strategies available to the child. While the strategies thechild can employ change with development, they also appear to beaffected by the information load presented in the array (Ak-shoomoff & Stiles, 1995a, 1995b; Stiles & Stern, 2001). Thesedata suggest that developmental change in visuospatial processingis protracted and that how children process and interpret informa-tion from visual arrays reflects an interaction between the infor-mation available in the array and the processing strategies appliedto the task of defining the structure of the pattern.

Visuospatial Processing in Children With PL

Across a wide array of spatial construction tasks, children rang-ing in age from 3 to 15 years showed evidence of both subtledeficit and development (Akshoomoff, Feroleto, Doyle, & Stiles,2002; Stiles & Nass, 1991; Stiles et al., 2006; Stiles, Stern,Trauner, & Nass, 1996; Stiles, Trauner, Engel, & Nass, 1997;Stiles–Davis, 1988). However, the profiles of deficit differ for theright hemisphere PL (RPL) and left hemisphere PL (LPL) groups.Preschool children with RPL have difficulty processing spatialconfigurations. As toddlers they fail to organize objects into sys-tematic spatial groupings (Stiles–Davis, 1988), and they havedifficulty reproducing model constructions (Stiles et al., 1996;Vicari, Stiles, Stern, & Resca, 1998). In the late preschool period,these children’s drawings are disorganized; while they can producethe separate parts of objects in their drawings, they fail to organizethem into a coherent whole (Stiles et al., 1997). However, in all ofthese tasks, deficits are most notable at ages when the task ischallenging for typical peers, and with development the accuracyof constructions improves. Further, while improvement is seen inthe products of the children’s spatial construction efforts, deficitsin processing, that is, in how they complete their constructions,persist. This pattern of deficit and development continues throughthe school-age period (Akshoomoff et al., 2002). Even on a task asbasic as face matching, subtle deficits are evident. While perfor-mance is well above chance, adolescents with RPL are less accu-rate than controls in matching faces (Stiles et al., 2006). Togetherthese data point to an early occurring visuospatial deficit amongchildren with RPL that affects configural processing. Significantcompensation is observed across development, but subtle deficitspersist throughout childhood.

Children with LPL also show evidence of deficit, but in manycases the impairments are less pronounced than those observed inthe RPL group. As toddlers, simple spatial grouping does notappear to be affected (Stiles–Davis, 1988), but there is evidencefor subtle spatial processing on block construction tasks. By age 4,children with LPL can reproduce simple block constructions asaccurately as typical age-matched peers, but the procedures they

Figure 1. Performance of adult stroke patients on the memory for hier-archical forms task. Patients with right hemisphere injury are impaired inreproduction of the global level of the form, while patients with lefthemisphere injury are impaired in reproduction of the local level. Reprintedfrom Neuropsychologia, 24(2), D. C. Delis, L. C. Robertson, and R. Efron,“Hemispheric Specialization of Memory for Visual Hierarchical Stimuli,”p. 206. Copyright 1986, with permission from Elsevier.

62 STILES ET AL.

use to complete their constructions are notably simplified (Stiles etal., 1996; Vicari et al., 1998). By age 5, they produce recognizabledrawings of simple objects and figures, but there are subtle differ-ences in their drawings that can manifest as either limited patterndetail or perseverative repetition of single elements. In the school-age period, children with LPL perform poorly on tasks requiringthem to copy a complex form (Akshoomoff et al., 2002). Finally,subtle deficits are also observed in face processing. Accuracy andreaction time for the children with LPL are intermediate betweenthose of children with RPL and typical controls. Together, the datafrom children with LPL suggest a subtle visuospatial processingdeficit. However, much of the data from this group of children isless diagnostic of the specific nature of the deficit than that ob-tained from the children in the RPL group. Their spatial processingis immature across a range of measures, but a specific localprocessing deficit is clearly defined on only a subset of measures.This may well be due to the structure of the tasks. Performance onconstruction tasks should be affected by impairment of eitherconfigural or featural processing, but many of the tasks used todate may place greater demands on configural processing, and thusit may be easier to compensate for deficit in local-level processing(e.g., 3–D block construction). What is needed is a task that isspecifically designed to place comparable demands on the config-ural and featural aspects of visuospatial processing. Such a taskwould provide the opportunity to obtain within-task evidence ofdifferential deficit associated with the laterality of the lesion site.

The current article extends and elaborates on our earlier work onvisuospatial development in children with PL by using a taskadapted from Delis and colleagues (Delis, Kiefner, & Fridlund,1988; Delis, Robertson, & Efron, 1986) designed to systematicallyevaluate configural and featural processing deficits associated withlateralized injury. Children were asked to reproduce from memorya series of hierarchical stimuli. The stimulus materials were de-veloped for use with children as young as age 5, and they thusinclude both letter and geometric form stimuli that vary systemi-cally in complexity on the basis of child norms (see Dukette &Stiles, 2001, for a complete description of the stimuli). The scoringsystem consists of two separate but cross-calibrated accuracyscales: one that assesses the accuracy in producing global-levelinformation and one that assesses local-level accuracy. Most im-portantly for the current study, our studies of typically developingchildren have shown that while overall performance improves withage, there are no systematic differences in children’s accuracy inproducing the global and local pattern level at any age. The designof this task should then allow us to detect differential impairmentfor processing the global or local levels of pattern information inchildren with PL.

Method

Data collection for the current study extended over more than adecade, covering much of the 1990s. At the onset of the study,participants ranged in age from preschool to late school ages. Asa result, we have compiled a large cross-sectional data set thatincludes a younger group (5–7 years old) and an older group (9–14years old). In addition, there was a small subset of children whowere seen at both ages. Data from both the cross-sectional andlongitudinal data sets are presented and, as will be evident, tell avery similar story. However, longitudinal data on special popula-

tions is rare, and we feel that it is important whenever possible topresent such data, even at the risk of some redundancy. Presenta-tion of the longitudinal study will be succinct.

Participants

The participants in the cross-sectional study included 38 chil-dren with PL (19 per group) and 24 typically developing children.Each patient had a single, unilateral lesion that was the result of aperinatal injury (in most cases, presumed to be the result of astroke). This was determined through clinical history and medicalrecord review, as well as through review of MRIs or CT scans (seeTable 1 for lesion descriptions) by the project neuroradiologist(John Hesselink), confirmed in consultation with the project neu-rologist (Doris Trauner). Children were excluded from the study ifthey demonstrated evidence of multiple lesions, diffuse damage, orconditions that can cause global brain damage (e.g., anoxia, viralinfection, encephalitis). Each of the groups (LPL, RPL, and con-trol) included a younger and an older age group. The youngergroup ranged in age from 5 to 7 years, and the older from 9 to 14years. Analysis of variance (ANOVA) revealed no differences inage across groups at either age point, Group (RPL, LPL, con-trol) ! Age (young, old); F(2, 56) " 1.50, p # .23; see Table 2.Participants in the longitudinal study included a subset of 21children from the cross-sectional study (6 with RPL, 8 with LPL,and 7 controls) who were tested at both age points.

As part of their participation in this longitudinal project exam-ining the effects of perinatal injury on cognitive development, allof the patients and controls underwent intelligence testing with anage-appropriate Wechsler Intelligence Test: Wechsler Preschooland Primary Scale of Intelligence—Revised (WPPSI–R), Wechs-ler Intelligence Scale for Children—Revised (WISC–R), WechslerIntelligence Scale for Children—Third Edition (WISC–III), orWechsler Intelligence Scale for Children—Fourth Edition (WISC–IV; Wechsler, 1974, 1989, 1991, 2003, respectively). Although nomatching strategy is ideal, in this study verbal IQ (VIQ) matchingwas selected for two reasons: (a) The target behaviors are spatial,and previous data from this population suggest that the two lesiongroups have distinct and persistent profiles of spatial deficit (Stileset al., in press; Stiles et al., 2005). Thus any global measure ofspatial ability is likely to reflect different underlying spatialstrengths and weaknesses for the two groups, making the datainherently noncomparable. (b) There is ample evidence that, de-spite early lesion-specific deficits in language acquisition, by age 6the children test within the normal range on standardized measuresof lexical and morphosyntactic mastery, and no lesion site-specificdeficits in language ability are present (Reilly et al., in press; Stileset al., in press; Stiles et al., 2005). Language matching thus appearsto be a more robust and less confounded basis for overall groupmatching in this study. Group comparisons of VIQ on the basis ofANOVAs revealed no significant differences among the threegroups of participants at either the older or younger ages: group(RPL, LPL, control), F(2, 59) " 1.84; Group ! Age (young, old)interaction, F(2, 55) " 0.49; see Table 2. In most cases the specificIQ instrument used for evaluation was appropriate for the child’sage at the time of experimental testing. However, as noted inTable 2, in a few cases testing was completed at only a single agepoint that did not coincide with their age at experimental testing.

63EARLY BRAIN INJURY AND VISUOSPATIAL PROCESSING

The IQ test results that corresponded most closely in time to theexperimental data point for each child are reported.

The children were also tested on the Beery–Buktenica Devel-opmental Test of Visual–Motor Integration (VMI). The VMI re-quires children to copy a series of geometric forms and provides ameasure of general visuospatial reproduction ability. Analysis ofthe VMI scores for the three groups revealed a significant effect ofgroup, F(2, 32) " 7.79, p # .002. Tukey Honestly SignificantDifference tests revealed that while the performance of both pa-tient groups was significantly below controls (RPL # controls, p #.02; LPL # controls, p # .002), the LPL and RPL groups did notdiffer (RPL " LPL, p $ .659).

All children used their preferred hand for drawing. Many chil-dren had hemiparesis contralateral to lesion site identified byneurological exam, and thus their preferred hand was ipsilateral totheir lesion. All children had normal or corrected to normal vision,as confirmed during their annual neurological examinations. No

motor or visual difficulties were present in the participants thatimpacted their performance on the drawing task.

Stimulus Materials

Each of the four memory reproduction stimuli were computer-generated and laser-printed. For each item, the model stimulus waspositioned in the center of an 8 1/2 in. ! 5 1/2 in. sheet of whitepaper, and the sheet was then laminated.

Hierarchical test stimuli. The stimuli used in this study weredeveloped as part of a separate study of typically developingchildren between the ages of 4 and 8 (see Dukette & Stiles, 2001,for a description of stimulus development). Children were testedwith four hierarchical stimuli. Each stimulus consisted of small,local-level elements (0.4 cm ! 0.3 cm) that were positioned in a5 ! 7 matrix to form the larger, global-level form (3.7 cm ! 2.5cm). As shown in Figure 2, two of the stimuli were constructed of

Table 1Lesion Information for Children in the Perinatal Focal Brain Lesion Groups

ParticipantBrain

hemisphere SeizureaLobe

involved Lesion description

3005 Right No TP Deep medial subcortical hemorrhage3006 Right No FTPO Porencephaly, posterior $ anterior3008 Right Yes FPO Infarction3022 Right Yes FTPO Infarction, small occipital3034 Right No FTP Porencephaly, small amount frontal3050 Right No FTP Lesion along the posterior sylvian fissure at the junction of three lobes3051 Right No F Infarction3063 Right Yes FTPO MCA infarction3064 Right No P Small porencephaly3504 Right Yes FTP Cortical dysplasia around sylvian fissure involving inferior frontal and superior temporal gyri3803 Right Yes FP Infarction3805 Right No FP Ventricular dilation and minor areas of increased signal intensity3806 Right Yes P Ventricular dilation, thin corpus callosum; later MRI indicated small bilateral hyperintensity3814 Right Yes P Centrum semiovale adjacent to the ventricle, ventricular dilation, subcortical only3828 Right No FPO Ventricular dilation, cystic cavity, parietal white matter hyperintensities3829 Right Yes FTP MCA infarction, dilation of frontal horn3856 Right Yes FTPO Subarachnoid hemorrhage3875 Right No Subcx Periventricular encephalomalacia3885 Right Yes FTP Dilation of the right lateral ventricle3002 Left Yes FTPO Infarction, maximum parietal; 34 wks premature3004 Left Yes FT Porencephaly, deep central volume loss3011 Left No F Periventricular cystic cavity, subcortical3016 Left Yes FTP Porencephaly, mostly temporal, small amount frontal3017 Left No T Deep anterior volume loss3018 Left No FTP Porencephaly, small amount frontal3032 Left No FTPO Atrophy, small amount frontal and occipital; primary lesion subcortical white matter3045 Left No Subcx Infarction involving the basal ganglia3056 Left No F Subcortical3059 Left Yes FTPO Infarction, porencephaly3065 Left No FTPO Ventricular dilation, entire hemisphere is small3802 Left Yes FTPO Hemiatrophy, porencephaly3804 Left No F Infarction3810 Left No F Infarction3812 Left Yes PTO Infarction3821 Left No Subcx Ventricular dilation; small cyst in subcortical white matter near lateral ventricle3849 Left No T Deep volume loss3886 Left Yes FPO Hemiatrophy, encephalomalacia, gliosis3895 Left Yes FTP Infarction

Note. TP " temporal parietal; FTPO " frontal temporal parietal occipital; FPO " frontal parietal occipital; FTP " frontal temporal parietal; F " frontal;P " parietal; FP " frontal parietal; Subcx " subcortical; FT " frontal temporal; T " temporal.a Denotes whether child has had a seizure during the post neonatal period.

64 STILES ET AL.

Table 2IQ Scores for Each of the Children in the Current Study

Participant Lesiona Ageb Gender IQ test VIQ PIQ FSIQ VMI

3005 Right 9.58 F WISC–R 115 133 127 913006 Right 7.58–9.42c M WISC–R 135 106 123 903008 Right 9.17 M WISC–R 90 95 91 873022 Right 6.17–8.17c M WPPSI-R 93 80 86 903034 Right 5.08 F WISC-R 131 108 123 973050 Right 6.50–8.16c M WISC–R 124 133 133 1013051 Right 6.33–10.91c M WISC–R 100 93 96 903063 Right 10.83 M WISC–III 78 70 71 773064 Right 5.42 M WPPSI–R 98 91 94 1023504 Right 9.92 M WISC–III 105 93 99 –3803 Right 10.08 M WISC–III 76 72 72 743805 Right 6.33–11.5c M WPPSI 109 95 102 833806 Right 6.08 F WPPSI 82 88 84 933814 Right 12.33 F WPPSI–R 87 104 94 1173828 Right 10.42 M WISC–III 119 77 98 753829 Right 6.92–9.16c M WISC–III 93 64 77 753856 Right 10.5 M WISC–III 79 58 66 813875 Right 10.75 F WISC–III 112 87 101 953885 Right 9.83 F WISC–IVd 102 63 81 673002 Left 5.08–8.33c M WISC–R 107 98 102 913004 Left 6.08c–9.08 M WISC–R 106 105 105 933011 Left 6.08c–9.08 M WISC–R 111 118 116 763016 Left 6.08–9.17c M WISC–R 85 88 85 963017 Left 6.00c–9.17 F WISC–R 106 104 105 1193018 Left 6.00–8.92c M WISC–R 120 102 113 933032 Left 6.33 F WISC–R 105 78 91 603045 Left 5.08–8.17c F WISC–R 137 92 118 923056 Left 5.25 M WISC–R 136 126 134 993059 Left 6.58 F WISC–R 86 81 82 1013065 Left 6.00–9.16c F WISC–R 114 92 104 1093802 Left 9.83 F WISC–R 98 88 92 823804 Left 10.42 M WISC–III 123 116 122 913810 Left 14.00 F WPPSI–R 107 124 116 1133812 Left 10.33 F WISC–R 110 115 113 753821 Left 5.25 M WPPSI 96 92 93 1113849 Left 11.33 F WISC–III 85 80 81 793886 Left 11.5 F WISC–III 81 83 81 –3895 Left 14.08 F WISC–III 82 83 81 –8007 Control 7.08 M WISC–R 130 115 126 1148014 Control 6.42–9.25c M WISC–R 131 123 130 928015 Control 5.00 F WPPSI–R 102 105 103 938016 Control 6.42 M WPPSI–R 97 91 94 978023 Control 9.33 F WISC–R 108 115 112 1238025 Control 7.50c–9.25 F WISC–R 118 102 112 1028036 Control 13.17 F WISC–R 120 124 125 1098037 Control 11.92 F WISC–R 108 123 117 1228040 Control 5.67 F WPPSI–R 112 102 108 1038048 Control 6.17 M WPPSI–R 93 109 101 968049 Control 5.67 F WPPSI–R 98 126 111 1038069 Control 5.67 F WISC–R 115 108 113 1128083 Control 7.10c–8.17 M WISC–R 98 101 100 1018086 Control 5.25 M WPPSI–R 103 105 105 1138095 Control 5.33 F WPPSI–R 111 104 108 958110 Control 6.18c–9.00 F WISC–III 107 115 112 1008119 Control 9.5 M WISC–R 123 109 119 –8125 Control 11.33 M WISC–R 109 111 111 –8139 Control 9.25 M WISC–R 113 112 114 1108150 Control 6.00 M WISC–R 109 105 108 1098155 Control 5.67c–8.50 M WPPSI–R 98 106 102 978169 Control 5.75c–8.50 M WISC–R 100 90 94 1038218 Control 5.25–8.08c F WPPSI–R 119 104 113 9910010 Control 9.6 M – – – – 88

Note. Dashes indicate that the data point was not available. VIQ " verbal IQ; PIQ " performance IQ; FSIQ " full scale IQ; VMI " Beery–BuktenicaDevelopmental Test of Visual–Motor Integration; WISC–R " Wechsler Intelligence Scale for Children—Revised; WPPSI–R " Wechsler Preschool andPrimary Scale of Intelligence—Revised; WISC–III " Wechsler Intelligence Scale for Children—Third Edition; WPPSI " Wechsler Preschool and PrimaryScale of Intelligence; WISC–IV " Wechsler Intelligence Scale for Children—Fourth Edition.a Indicates which hemisphere of the brain had a lesion or whether participant was in the control group. b Age in years at time of experimentaltest. c Indicates children who were also included in the longitudinal study and which session was added. d VIQ and PIQ were estimated on the basis ofthe VMI and the perceptual reasoning index.

65EARLY BRAIN INJURY AND VISUOSPATIAL PROCESSING

letters (the D of Ls and the Y of Bs), and two were constructed ofgeometric forms (the pi symbol of triangles and the square ofpluses). Dukette and Stiles (2001) demonstrated that two stimuliwere easier for children to reproduce; children were more accuratewith the Y of Bs and the square of pluses. Further, performance onthe two easier stimuli was comparable, as was performance on thetwo more difficult forms.

Procedure

Pretest/training. To confirm their understanding of task in-structions, children were asked to reproduce up to six simplehierarchical items. Each item consisted of simple geometric forms(e.g., dots, Xs, dashes) arranged in a horizontal, vertical, or obliqueline. Only children who were successful on this pretest proceededto the experimental condition.

Memory experiment. The memory task consisted of four trials,one for each hierarchical stimulus. On each memory trial, onehierarchical stimulus was presented and children were given 10 sto study it. Next, a 30-s distractor task in which the children wereinstructed to order a three-card picture sequence (e.g., a child infront of an easel: putting on an apron, dipping a paintbrush inpaint, admiring her drawing) was introduced. Finally, the childrenwere given a felt tipped pen and an 8 1/2 in. ! 5 1/2 in. blank sheetof white paper and asked to reproduce the model form frommemory. They were given unlimited time to complete their draw-ings. The same procedure was repeated for each of the fourmemory trials.

Scoring

Two independent raters scored the overall accuracy of all draw-ings and evaluated the drawings for specific error types. Raterswere unaware of the age, gender, or group of the participants.Interrater reliability was above 90%, and any disagreements wereresolved by consensus of the two raters.

Overall accuracy of global- and local-level reproduction. Theoverall accuracy of the global and local levels of each drawing wasscored separately with two different but comparable 6-point (0–5)ordinal scales. Each drawing received two scores: one for theglobal-level accuracy and one for the local-level accuracy (seeDukette & Stiles, 2001, Appendix B, for a detailed description ofthe scoring categories for the global- and local-level scales). Asshown in Table 3, for the global scale, a low score would beassigned for a configural form of the wrong shape. A midrangescore would be given for a correct but nonconfigural global shape.

Figure 2. Model forms for the child memory reproduction task. From“The Effects of Stimulus Density on Children’s Analysis of HierarchicalPatterns,” by D. Dukette and J. Stiles, 2001, Developmental Science, 4(2),p. 237. Copyright 2001 by Blackwell Publishers Ltd. Reprinted withpermission.

Table 3Scoring for Global- and Local-Level Accuracy

Score Global-level accuracy Local-level accuracy

0 Scribble. Scribble.Randomly placed local elements. One form.Incorrect nonconfigural form.

1 Incorrect global form, configured from local elements. Incorrect local elements (must be at least two elements).Attempt to indicate elements but no real local-level forms (e.g., dashed

lines).2 Basic form but greatly simplified or distorted. # 50% of correct number of elements (must be discrete and

recognizable).“Overdrawing”—local elements drawn on top of inaccurate

nonconfigural form.aAt least one element must be correct.

3 Accurate global form—configural or nonconfigural.a All elements recognizable.Orientation off more than 20 degrees. $ 50% of correct number present.Spacing of elements may be distorted (non-uniform or irregular). $ 50% of elements must be correct.

$ 50% oriented correctly.4 Accurate global form, must be configural. All elements accurate and uniform in size.

Adequate, uniform spacing (no more than four forms may touch). Adequate spacing between elements (no more than four may touch).Elements oriented within 10 degrees. Elements oriented within 10 degrees.Generally well drawn.

5 Accurate configural global form. All elements accurate and well drawn.Accurate spacing between all elements. All elements correctly oriented.Accurate orientation. Accurate number of elements.Accurate number of local elements. Accurate spacing.

Note. From “The Effects of Stimulus Density on Children’s Analysis of Hierarchical Patterns,” by D. Dukette and J. Stiles, 2001, Developmental Science,4 (2), p. 249–250. Copyright 2001 by Blackwell Publishers, Ltd. Reprinted with permission.a The global accuracy scoring was modified slightly in this study to correct an inconsistency in the original system. In the original system, the principalcriterion for a score of 3 for both global and local accuracy was accurate representation of the form for the target level. Yet production of a correct,nonconfigural global form, either alone or in the case of overdrawing, was given a score of 2 in the original system. That inconsistency was corrected inthis study. If the child produced an accurate global form (e.g., a Y, for the Y of Bs), a score of 3 was awarded.

66 STILES ET AL.

A higher score would require both a correct and configured globalshape. For the local scale, a low score would be assigned for areproduction of multiple but incorrect or unrecognizable elements.A midrange score would be given for a few correct elements, anda higher score for many correct elements.

Specific errors of hierarchical form reproduction. While theoverall accuracy measures provide a general assessment of thechildren’s ability to reproduce the global and local levels of thehierarchical patterns, they do not allow for examination of thespecific kinds of errors children make. Five additional error anal-yses were designed to examine whether there is evidence forsystematic differences in how the children in the different groupsproduced the forms (note: examples of each error type and subtypeare presented in the Results section):

1. Local Errors of Omission or Element Substitution (LE):An LE error was scored when local-level elements wereomitted entirely or when the wrong local-level form wasproduced.

2. Global Errors of Omission or Global Form Substitution(GE): A GE error was scored when an unrecognizableglobal-level form or the wrong global-level form wasproduced.

3. Local Element Orientation Shift (LOS): An LOS errorwas scored when orientation of a local element wasshifted to conform to the orientation of the segment of theglobal-level form of which the element was a part. Eval-uation of element orientation accuracy depends on accu-rate production of elements. Thus, this error type wasscored only for reproductions receiving a score of 2 ormore on the local-level scale.

4. Global Segment Orientation Shift (GOS): A GOS errorwas scored when the orientation of a segment of theglobal form was distorted to conform to the orientation ofthe local-level elements of which the segment was com-posed. Evaluation of segment orientation accuracy de-pends on accurate production of the global form. Thus,this error type was scored only for reproductions receiv-ing a score of 2 or more on the global-level scale.

5. Scaffolding and Linking (S-L): An S-L error was scoredeither when a child began by drawing the outline of all orpart of the global form and then added the local elementsaround this “scaffold,” or when a child conjoined, orlinked, a minimum of three local elements in a smoothconcatenation such that a continuous segment of theglobal form was created.

Results

Cross-Sectional Study

The results of the cross-sectional study revealed different pat-terns of performance for the three groups. Differences were ob-served in the accuracy of reproducing the global and local levels ofthe hierarchical stimuli. Performance differences were also ob-served among members of the RPL group for the letter and formstimuli. Analysis of specific types of errors for each group wasconsistent with the overall global–local accuracy analysis. Chil-dren with RPL were more likely to make global-level errors, whilemore local-level errors were observed in children with LPL.

Overall accuracy. The accuracy data were analyzed with afive-variable mixed-design ANOVA. Group (RPL, LPL, control)and age (young, old) were between-participants variables, andlevel (global, local), complexity (simple, complex), and type (let-ter, form) were within-participant variables. Results revealed sig-nificant effects of group, F(2, 56) " 6.74, p # .002, and age, F(1,56) " 54.45, p # .000. There were also significant Group ! Level,F(2, 56) " 5.44, p # .007, and Group ! Type, F(2, 56) " 3.58,p # .034, interactions.

Differences were observed among the groups in global- andlocal-level reproduction accuracy (see Figure 3). Consistentwith earlier studies, global- and local-level accuracy were com-parable for controls. Planned comparisons ( p # .05, withBonferroni correction for familywise error) showed that theRPL group was more accurate on local elements than globalforms and the LPL group was more accurate on the globalaspect than the local. The findings on the overall accuracy for theRPL and LPL groups suggest selective deficits in global- andlocal-level processing, respectively. Further, the children’s perfor-mance mirrored that of adults with focal lesions on a similar task(Delis et al., 1986).

Correlation and regression analyses examined the associationbetween global and local performance accuracy for each group(see Figure 4). The association between global and local accuracyfor the controls was high, r " .83, p # .000; r2 " .686. Theassociation for the RPL group was also significant, r " .71, p #.001; r2 " .505, suggesting that while RH injury compromisesglobal-level processing, local performance is consistently high. Aweaker pattern of association was observed for the LPL group, r ".45, p # .053; r2 " .203, suggesting greater variability within thatgroup. While performance on local-level reproduction was consis-tently low, it did not predict performance on global-level repro-duction. Some children with LPL did well on global, others didnot.

Finally, the Group ! Type interaction was significant (seeFigure 5). Planned comparisons ( p # .05, with Bonferroni correc-

3.5

3

2.5

2

Mea

n A

ccu

racy

(0-

5)

RPL LPL Control

GlobalLocal

**

Figure 3. Analysis of data from the global- and local-level accuracyanalyses shows significant differences in the accuracy of performance atthe two levels. Children with right hemisphere perinatal focal brain lesions(RPL) were significantly more accurate in reproducing the local than theglobal level, while children with left hemisphere perinatal focal brainlesions (LPL) were significantly less accurate reproducing the local thanthe global level. Asterisks indicate a statistically significant difference (p #.05) between adjacent bars (i.e., global # local for RPL and global $ localfor LPL).

67EARLY BRAIN INJURY AND VISUOSPATIAL PROCESSING

tion for familywise error) showed that while neither the controlsnor the LPL group differed in their accuracy with the letter andform stimuli, the RPL group was significantly more accurate withthe letters. Further, while both the LPL and RPL groups’ perfor-mance was worse than that of controls’ on the form stimuli, onlythe LPL group differed from controls on the letter stimuli. Thesefindings suggest that the RPL group, but not the LPL group, may

benefit when the reproduction task involves very familiar, fre-quently produced elements, and suggest a possible verbal strategyfor these items. However, this finding should be treated withcaution. Figure 6 shows the pattern of performance for each groupon each of the four hierarchical stimuli. There is very little differ-ence in the performance of either the controls or the LPL groupacross the four stimuli. The LPL group was more accurate onglobal than local on all four stimuli, and controls did equally wellon the two levels for all stimuli. However, while the RPL groupwas more accurate on local than global for all stimuli, the effect ismost pronounced for the D of Ls and the square of pluses. Theapparent advantage for letter stimuli is actually attributable to thecomparatively better global performance on the Y of Bs and theirworse performance with local on the pi symbol of triangles. Thus,the advantage observed for this group appears to be attributable toperformance differences on individual stimuli rather than to aspecific advantage for letter stimuli. When the stimulus was simpleand was a letter (Y of Bs), the RPL group benefited, but when it wasa complex form (pi symbol of triangles), performance suffered.

Analyses of specific error types. The percentage of children ineach group (RPL, LPL, control) committing each of the five errortypes was calculated and compared by means of paired sample ttests. Differences were observed between the groups for each errorcategory. Figure 7A shows the distribution of global errors. Morechildren in the RPL group made global errors than did those in thecontrol group, t(41) " 2.25, p # .03. The performance of the LPLgroup was intermediate; they did not differ from either the con-

Figure 4. The association between global- and local-level accuracy performance differed among the threegroups. For controls, the association was robust (r " .83, p # .000; r2 " .686), and it was also strong amongthe children with right hemisphere perinatal focal brain lesions (RPL; r " .711, p # .001; r2 " .505). However,only a weak association was observed for those with left hemisphere perinatal focal brain lesions (LPL; r " .451,p # .053; r2 " .203). While the LPL group’s local-level accuracy was uniformly low, its global-level accuracywas variable.

Figure 5. Mean accuracy by each group on the letter and form stimuli.While neither the group with left hemisphere perinatal focal brain lesions(LPL) nor the controls performed differently on the two stimuli, the groupwith right hemisphere perinatal focal brain lesions (RPL) was significantlymore accurate on the letter stimuli. Asterisk indicates a statistically signif-icant difference (p # .05) between adjacent bars (i.e., letter and form).

68 STILES ET AL.

trols, t(41) " 0.80, p # .43, or the RPL group, t(36) " 1.32, p #.17. Figure 7B shows the distribution of local errors. Althoughchildren in both lesion groups made more errors than did controls,the magnitude of the difference was greater for the LPL group,t(41) " 3.22, p # .003, than for the RPL group, t(41) " 2.59, p #.013. The children in the RPL group tended to distort the orienta-tion of the global-level segments (GOS errors), thus distorting theoverall configuration (see Figure 8A). More children in the RPLgroup made GOS errors than did either controls, t(41) " 2.00, p #.05, or children in the LPL group, t(36) " 2.23, p # .032. Bycontrast, both the RPL group and the controls tended to makeerrors in the orientation of local elements (see Figure 8B), but theywere rarely made by children in the LPL group, LPL vs. control,t(41) " 1.95, p # .058; LPL vs. RLP, t(36) " 1.69, p # .099.These data suggest that while reorienting local-level elements tothe plane of the segment being constructed may assist most chil-dren, it is not a strategy that is useful for children in the LPL group.

Finally, as shown in Figure 8C, the strategies of element linkingand scaffolding were more common among children with RPLlesions than among controls, t(41) " 2.20, p # .03. The perfor-mance of the LPL group was intermediate and did not differ fromcontrols, t(41) " 1.51, p # .14, or the RPL group, t(36) " 0.31,p # .76.

Longitudinal Study

The results of the longitudinal study were very similar to thoseof the cross-sectional study. The sample sizes in the longitudinalstudy were considerably smaller than in the cross-sectional study,thus limiting the range of possible analyses, particularly for theerror analyses that cannot accommodate repeated measures data.However, the results of the overall accuracy ANOVA for thelongitudinal study mirrored the findings observed in the cross-sectional study.

Figure 6. Performance of the three groups from the cross-sectional study on each of the four stimuliindividually. While the performance of the group with left hemisphere perinatal focal brain lesions (LPL; seepanel B) and the controls (see panel C) did not differ significantly across items, item-specific differences werenoted for the group with right hemisphere perinatal focal brain lesions (RPL; see panel A). Specifically, for theRPL group, local- and global-level accuracy on the simple letter stimulus (Y of Bs) was high, while on theremaining three stimuli their performance was significantly better on local than global. These findings suggestthat interpretation of the stimulus type effect (i.e., better performance on letters than geometric forms) for thisgroup should be viewed with some caution. (Y-B " global Y/local B; D-L " global D/local L; S-P " globalsquare/local plus; P-T " global pi symbol/local triangle.)

69EARLY BRAIN INJURY AND VISUOSPATIAL PROCESSING

The accuracy data were analyzed with a three-variable mixed-design ANOVA. Group (RPL, LPL, control) was the between-participants variable, and age (young, old) and level (global, local)were within-participant variables. There were differences amongthe groups in the reproduction accuracy at the global and locallevels. The significant Group ! Level interaction, F(2, 18) " 5.10,p # .018, mirrored the findings of the cross-sectional analysis.Planned comparisons ( p # .05, with Bonferroni correction forfamilywise error) showed that while neither the controls nor theLPL group differed in accuracy at the global and local levels, theRPL group was significantly more accurate on the local than globallevel.

Discussion

The results of this study confirm earlier findings of visuospatialdeficits following PL. Children in both the RPL and LPL groupswere significantly less accurate than controls in their reproductionsof hierarchical form stimuli, as indexed by both the overall accu-racy measures and by the measures of specific errors. Children inthe patient groups were matched with controls for age and IQ andwere successful in reproducing recognizable copies of the first 10items on the VMI. Thus, the deficits observed in the patient groupscannot be attributed to a difference in either general intellectualfunctioning or to deficits in visuomotor control. While there was asignificant effect of age, there was no evidence of an Age ! Groupinteraction, suggesting improvement in performance with age forall of the children in the study. A very similar pattern of results wasobserved for children in the smaller, longitudinal study, thusconfirming the core findings in a within-participant design. Thesefindings suggest that while early injury does affect visuospatialprocessing, children appear to be able to compensate, at least in

part, for their deficits. By the late school-age period, performanceimproves significantly and evidence of only subtle deficits re-mains. In addition to illuminating these general findings of subtlevisuospatial deficits associated with early brain injury, this studyprovided clear evidence of a dissociation between lesion lateralityand specific type of deficit. Children with RPL were impaired inglobal-level accuracy, while children with LPL were impaired atthe local level.

Spatial Deficits and LPL

Our earlier work with the LPL group suggested subtle visuo-spatial processing deficits. In most of our earlier studies, thedeficits observed among the LPL group were less pronounced thanthose of the RPL group, and documentation of specific deficits infeatural processing was less consistent across studies. The currentstudy departs from the earlier work in that it documents within asingle task, carefully matched for global and local processingdemands, a double dissociation in global- versus local-level pro-cessing for the LPL and RPL groups.

Importantly, the local processing deficit among the LPL groupwas pronounced. The magnitude of the difference between theirlocal-level accuracy was as great as the magnitude of the globalprocessing difference observed for the RPL group, and it persistedover time. Further, significantly more children with LPL madelocal-level errors of omission or substitution than did children withRPL or controls. Children with LPL also rarely made errorsinvolving misorientation of local-level elements. This error typewas frequent among both children with RPL and controls andsuggests the use of strategies involving alignment of local ele-ments to assist in reproduction of the global structure. The absenceof such strategies among the LPL group may be indicative of their

Figure 7. Omission and substitution errors are shown for each group. Examples of error types are shownbeneath each figure. (A) Global-level omission and substitution errors were significantly more common amongchildren with right hemisphere perinatal focal brain lesions (RPL) than controls, and the performance of thosewith left hemisphere perinatal focal brain lesions (LPL) was intermediate and did not differ from either the RPLgroup or controls. (B) Both the children with LPL and those with RPL made significantly more errors of localomission or substitution than did controls, and the two patient groups did not differ.

70 STILES ET AL.

deficits in local-level processing. Finally, consistent with controlsand in contrast to the RPL group, children with LPL rarely madeerrors involving global segment distortion. This set of findings isconsistent with reports of early left lateralization for local-levelprocessing among typically developing infants (Deruelle & deSchonen, 1991, 1998; Deruelle & Fagot, 1997) and suggests thatthe LH specialization for local, or featural level, processing beginsto emerge very early in development.

However, it is also important to note that on measures ofassociation between global and local processing, the LPL groupwas less consistent than the other two groups. While the RPLgroup and controls showed strong associations between measures

of global- and local-level accuracy, only a weak association wasobserved for the LPL group. This finding is accounted for bygreater variability in global-level accuracy among children in thisgroup. While the LPL group had consistently low performance onlocal accuracy, their global-level accuracy was more mixed.

The particular demands of the memory reproduction task mayaccount for the more variable performance among the LPL groupon global-level accuracy. For typically developing children, thetask places comparable demands on global- and local-level pro-cessing, as evidenced by the strong association between global-and local-level accuracy. Among children with RPL, at all agesglobal processing is impaired relative to local processing, but

Figure 8. Orientation and element concatenation errors are shown for each group. Examples of error types areshown beneath each figure. (A) Global segment errors were significantly more common among children withright hemisphere perinatal focal brain lesions (RPL) than among controls or children with left hemisphereperinatal focal brain lesions (LPL). The LPL group did not differ from controls. (B) Children with RPL andcontrols made more errors of local substitution than did children with LPL. This suggests that the strategy ofreorienting local elements to conform to the global shape did not facilitate performance in the LPL group. (C)Children with RPL were significantly more likely than controls to use strategies involving linking of elementsto form the global configuration. Children with LPL were intermediate and did not differ from controls orchildren with RPL.

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because there is overall improvement in performance with devel-opment, the association between global and local processing iscomparatively strong. By contrast, the local-level processing def-icit observed for children with LPL shows only a weak associationwith global accuracy. This dissociation likely reflects individualdifferences in the strategies children adopted to compensate fortheir local processing deficits. For example, in the face of diffi-culties in reproducing local elements of the configured form, somechildren simply produced a single, accurate but unconfiguredglobal form, while others produced an accurate global configura-tion but created it from simplified local elements (e.g., creating aglobal square from a set of dashed lines). Thus, these childrendemonstrate facility with global processing by ignoring or dimin-ishing the local processing demands. However, other childrenattempted to produce the configured global form by using the moredifficult, matched local elements. This approach required them togenerate a series of complex local elements, thus taxing their areaof weakness. For these children, their deficits in local-level pro-cessing may have affected their ability to produce an accurateglobal form. This variation in strategies may account for thelowered association between global and local processing observedamong children in the LPL group.

Spatial Deficits and RPL

A strong dissociation in reproduction accuracy was observedin children with RPL, in that they were more accurate with thelocal-level elements than with the global form. Further, signif-icantly more children with RPL made global-level errors ofomission or substitution and were more likely to distort theglobal shape. These findings are consistent with studies thatreport the early emergence of lateralized differences in config-ural processing and suggest early commitment of the RH toconfigural processing. Further, they converge on findings fromstudies of children with early visual deprivation in suggestingthat there are limitations on the capacity of the LH to compen-sate for injury to the RH (Le Grand, Mondloch, Maurer, &Brent, 2004). Le Grand et al. (2004) reported that brief periodsof left monocular deprivation results in subtle long-term deficitsin configural processing. They note that the temporal visualfield pathways develop ahead of the nasal pathways, and thusinformation to the right eye derives primarily from the temporalleft visual field and is projected almost exclusively to the RHvisual areas, and vice versa. Given this pattern, early monoculardeprivation essentially eliminates input to the contralateral vi-sual cortex. Without input, the early maturing RH visual systemfails to develop the typical dominance for configural process-ing, and the nondeprived LH cannot fully compensate for theRH deficits. The current data from the children with PL areconsistent with these findings. Perinatal injury to the RH visualsystem results in persistent deficits of configural processing,suggesting, as observed in the Le Grand study, only a limitedcapacity of the LH to compensate for early RH deficits (Stileset al., 2003). Conversely, if the RH is committed very early toa particular mode of processing, it may retain only limitedcapacity to organize differently to accommodate early injury tothe LH.

Summary and Conclusions

The results of this study confirm and extend earlier work exam-ining the effects of lateralized perinatal focal brain injury onvisuospatial development. Regardless of the site of injury, childrenwith PL show signs of subtle impairment that persists throughchildhood. The type of deficit differs depending on lesion lateral-ity. Children with RPL have global-level processing deficits, whilechildren with LPL have local-level processing deficits. These dataare consistent with studies of typically developing infants and withdata from children with early visual deprivation, suggesting thatthe basic, lateralized organization of the human visual system isestablished early. These findings have important implications forunderstanding visuospatial development in children with perinatalbrain injury. Specifically, the evidence for early commitment ofthe neural systems for visuospatial processing suggests that earlyinjury should result in permanent deficits. However, the protractedterm of visuospatial development may serve to mitigate the effectsof early neural and cognitive commitment. These issues go to theheart of the debate over the role of plasticity in brain development.Children in our studies show subtle, specific visuospatial process-ing deficits, but they also show evidence of considerable develop-mental improvement and capacity for compensation.

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Received May 23, 2006Revision received May 30, 2007

Accepted June 5, 2007 !

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