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Hemispheric specialization for local and global processing of hierarchical visual stimuli in chimpanzees (Pan troglodytes)
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Pergamon
Neuropsycholo`ia\ Vol[ 24\ No[ 2\ pp[ 232Ð237\ 0886 Þ 0886 Elsevier Science Ltd[ All rights reserved Printed in Great Britain 9917Ð2821:86 ,06[99¦9[99
PII] S9917Ð2821"85#99978Ð8
Hemispheric specialization for local and global processing of hierarchical visual stimuli in chimpanzees "Pan troglodytes# WILLIAM D[ HOPKINS Department of Psychology\ Berry College\ P[O[ Box 384908\ Mount Berry\ GA 29038!4918\ U[S[A[ "Received 1 April 0885^ accepted 11 July 0885#
Abstract*This study examined laterality in global and local processing of hierarchical compound stimuli in seven chimpanzees "Pan tro`lodytes#[ A divided visual half!_eld paradigm was used that allowed for unilateral presentation of compound stimuli to either the left or right hemisphere[ Comparison stimuli di}ering on the basis of their global con_guration\ local elements or both features followed sample stimulus presentation[ Subjects were required to accurately discriminate the comparison stimuli on the basis of these features relative to the sample stimulus[ No laterality e}ects were found for accuracy^ however\ for reaction time\ a signi_cant interaction was found between visual _eld and processing mode[ An overall right visual _eld advantage was found for local processing but no visual _eld di}erences for global processing[ The overall results are consistent with previous _ndings in humans and suggests homologous lateralization in chimpanzees and humans[ Þ 0886 Elsevier Science Ltd[ All rights reserved[ Key Words] global:local processing^ hierarchical compound stimuli^ chimpanzee[
tachistoscopically presented hierarchical compound stimuli unilaterally and compared performance between hemispheres when subjects are required to respond on the basis of the global con_guration or local elements of the stimulus[ Hierarchical compound stimuli are typically larger stimuli comprised of smaller elements that are either identical or di}erent in appearance from the shape of the larger stimulus[ An example of four hierarchical stimuli is depicted in Fig[ 0[ As can be seen\ the larger Arabic letters {H| and {L| can be constructed from the smaller letters[ Some have suggested that the right hemisphere is superior in pro! cessing global aspects of hierarchical compound stimuli while the left hemisphere is superior in processing local elements and there is empirical evidence to support this dichotomy ð13\ 17\ 29Ł[ For example\ in human intact subjects\ Martin ð13Ł presented hierarchical stimuli to either the left or right visual half!_eld and required sub!
Introduction Recent studies clearly suggest the presence of hemispheric specialization in nonhuman species ð0\ 21Ł[ For example\ in nonhuman primates\ there is evidence of population! level hand preferences ð5\ 05\ 12\ 14\ 21Ł\ asymmetries in visualÐspatial processing\ perception and production of facial expressions ð00\ 02\ 06\ 15\ 20Ł and in cognitive functions ð01\ 03\ 08\ 16Ł[ These cumulative results seri! ously challenge the long held belief that hemispheric spe! cialization is unique to humans ð2\ 4\ 24Ł[ A fundamental theoretical and empirical question that remains is whether the asymmetries observed in animals are hom! ologous to those observed in humans or whether they represent species!speci_c adaptations[ One way in which the human left and right hemispheres have been dichotomized has been in their propensity to process stimuli that di}er on the basis of either their global con_guration or local elements[ To assess this model of hemispheric specialization\ investigators have
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Address for correspondance] Department of Psychology\ Berry College\ P[O[ Box 384908\ Mount Berry\ GA 29038!4918\ U[S[A[ "Also at Yerkes Regional Primate Research Center\ Emory University\ Emory University\ Atlanta\ GA 29211\ U[S[A[#
L L L L L LLL L L L L
H H H H HHHH
H H H H H HH H H H H H
(1) (2) (3) (4) Fig[ 0[ Stimuli used in the experiment[
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W[ D[ Hopkins:GlobalÐlocal processing and laterality images
jects to report the local elements or global con_guration of the sample stimulus[ Subjects showed a right visual _eld advantage in reaction time when required to report the local elements of the stimulus[ No visual _eld di}er! ences were found in processing the global attributes of the stimuli[ Clinical studies support the dichotomy in hemispheric specialization and global:local discrimi! nation[ For example\ Delis et al[ ð3Ł asked patients with right and left hemisphere lesions to draw hierarchical compound stimuli[ Patients with right hemisphere lesions tended to draw the global aspects of the stimulus while patients with left hemisphere lesions tended to draw the local elements of the stimulus[ From a comparative perspective\ very little is known about the processing of hierarchial compound stimuli[ Recently\ Hopkins and Washburn ð10Ł have reported that chimpanzees exhibit a global!to!local precedence in the processing of hierarchical compound stimuli while rhesus monkeys do not[ Global!to!local precedence refers to performance in which subjects respond more quickly or more accurately to global aspects of compound stimuli compared to their local features[ Fagot and Deruelle ð7Ł reported the lack of a global!to!local precedence in the processing of hierarchical compound stimuli in a sample of 7 baboons while human subjects tested with the same stimuli did show the precedence[ Notwithstanding the lack of global!to!local precedence in baboons\ the baboons did discriminate stimuli that di}ered on the basis of their global con_guration when presented to the left visual!_eld\ suggesting a right hemisphere advantage[ No hemispheric advantages were reported in the processing of local aspects of these hierarchical stimuli[ The focus in this study was to determine whether the left and right cerebral hemispheres of chimpanzees di}erentially process hierarchical compound stimuli that di}er on the basis of their global con_guration\ local features or both attributes[ Based on _ndings by Martin ð13Ł in human subjects and those reported by Fagot and Deruelle ð7Ł\ I hypothesized that chimpanzees would dem! onstrate a right visual _eld advantage in processing the local elements of a hierarchical compound stimulus and a left visual _eld advantage when processing the global aspects of hierarchical compound stimuli[ For hier! archical stimuli di}ering on both global and local cues\ no visual _eld di}erences were predicted because subjects could utilize either cue to respond correctly on a given trial[
Methods Subjects Seven chimpanzees "Pan tro`lodytes#\ including _ve males and two females\ ranging from 6 to 09 years of age served as subjects[ All seven chimpanzees were raised in captivity at the Yerkes Regional Primate Research Center following standard nursery protocol for great apes ð0Ł[
Apparatus The basic test system used is referred to as the Language Research Center Computerized Test System "LRC!CTS# and has been described in detail elsewhere ð23Ł[ Each test system consisted of a personal computer "275!compatible#\ a 02!in[ color monitor\ and an analog joystick[ Food reinforcement was delivered by the experimenter by handing the food through the cage to the chimpanzee[
Stimuli The stimuli used are depicted in Fig[ 0 and are one set of stimuli that have been previously employed in our comparative visual perception studies of hierarchical compound stimuli in monkeys and chimpanzees ð10Ł[ The larger stimuli were 2[64 cm×1[4 cm in dimension[ The individual element features were 5 mm×5 mm with 0 mm spaces separating individual fea! ture within a larger stimulus[ The stimuli were white and pro! jected on the black background of the computer monitor[
Divided visual _eld task Prior to the onset of testing\ all subjects were trained to reliably use the joystick test system and perform a number of cognitive tasks including simultaneous and sequential matching! to!sample ð11\ 22Ł[ In this study\ a sequential matching!to!sam! ple paradigm presented within a divided visual!_eld "DVF# format was employed[ Use of the DVF testing format allowed for unilateral presentation of visual stimuli and therefore assess! ment of hemispheric specialization in neurologically intact sub! jects[ The general DVF testing procedure has been described in detail elsewhere ð07\ 19Ł[ At the beginning of each trial\ a cursor "a {¦| sign\ 8 mm×8 mm# and a _xation point "0 cm in diam! eter# appeared on the computer monitor[ The _xation point was positioned in the center of the computer monitor while the cursor was randomly positioned on the screen[ In order to view the screen\ subjects had to look through a viewport that separated the monitor from the cage[ The viewport was metal\ 49 cm in length and shaped like a rectangular funnel[ The wide end of the viewport was 26 cm×15 cm and _tted squarely over the computer monitor[ The narrow end of the viewport was 04 cm×5 cm with two eye holes cut equidistant from each other[ The eye holes were 1[4 cm in diameter[ The chimpanzees had to look through the eye holes to see the computer monitor[ The viewport allowed for control of the distance that each subject maintained from the _xation point each trial\ a necessary con! dition for assurance of unilateral presentation[
Procedure Each trial\ subjects were required to move their cursor to the _xation point displayed in the center of the computer monitor[ If this condition was met\ then a sample stimulus was presented for 099 msec either to the left or right side of the _xation point[ A 099 msec presentation duration precluded bilateral overlap in stimulus presentation due to saccadic eye movements ð25Ł[ The sample stimulus was one of the four stimuli displayed in Fig[ 0[ The inside edge of the sample stimulus was laterally placed at a visual angle of 5 degrees from the _xation point[ After sample stimulus presentation\ the sample stimulus was erased from the monitor and two comparison stimuli appeared equidistant from the _xation point[ One comparison stimulus was 4 cm above the _xation point and one was 4 cm below the _xation point[ The positive comparison stimulus was identical
Results The accuracy and response time data were analyzed using a complete within!subjects analysis of variance "ANOVA#[ Test session ð0\ 1Ł\ visual half!_eld "LVF\ RVF# and problem type "GLOBAL\ LOCAL\ BOTH# were the independent variables of interest[ A priori plan! ned comparisons in performance between the LVF and RVF for each problem were speci_ed in the ANOVA model[ Overall\ no signi_cant main e}ects or interactions were found for the accuracy data[ The mean percentage correct for the LOCAL\ GLOBAL and BOTH problems were 54)\ 40) and 45)\ respectively[ For the response time data\ signi_cant main e}ects for visual half!_eld ðF"0\5# 6[43\ P³9[93Ł and problem ðF"1\01# 4[08\ P³9[93Ł were found[ A signi_cant two!way interaction was found between visual half!_eld and problem ðF"1\01# 3[03\ P³9[94Ł and a signi_cant three!way interaction was found between test session\ problem and visual half!_eld ðF"1\01# 3[44\ P³9[93Ł[ Depicted in Fig[ 1 are the mean response times for each visual half! _eld and problem type[ The a priori contrasts indicated
1300 1250 1200 1150 1100 1050 1000 950 900 850 800 750 700
234
Local Global Both
LVF
RVF
Visual half-field
Fig[ 1[ Mean response times as a function of problem type and visual half!_eld[
a signi_cant di}erence in response between the LVF and RVF for the LOCAL problems ðt"5# 3[09\ P³9[995Ł[ No overall visual half!_eld di}erences were found for the GLOBAL and BOTH problems[ These _ndings account for the signi_cant interaction found between problem type and visual half!_eld[ With respect to the three!way interaction between test session\ visual half!_eld and problem type\ the data were transformed to simplify the interpretation of this result[ For each subject\ the mean response for the LVF was subtracted from the mean response time for the RVF within a test session and between problem types[ This resulted in either negative and positive di}erence scores with positive values re~ecting a RVF advantage and negative values re~ecting a LVF advantage[ Values on or about zero would re~ect either a slight or no visual _eld advantage[ The di}erence scores were subjected to a within!subject design ANOVA with test session and problem type as the independent variables[ A signi_cant two!way interaction was found between test session and problem type ðF"1\01# 3[44\ P³9[93Ł[ The mean di}er! ence score for each problem type and test session can be seen in Fig[ 2[ For the LOCAL problems\ a consistent RVF advantage was found between test sessions 0 and 1\ although the magnitude of this e}ect increased from session 0 to 1[ In contrast\ within test session 0\ essentially 350
Difference score (RVF-LVF)
to the sample stimulus while the alternative stimulus was a foil[ The foil stimulus was always one of the remaining three stimuli comprising the stimulus library[ A correct response was rec! orded when subjects moved their cursor to the positive com! parison stimulus[ Incorrect responses were recorded when the subjects moved their cursor to the foil[ Based on which com! parison stimuli were displayed\ there were three possible types of perceptual discrimination problems that could occur on a given trial[ LOCAL problems were those in which the two comparison stimuli di}ered in their local elements "Stimulus 0 and 2\ or 1 and 3#[ GLOBAL problems were those in which the two comparison stimuli di}ered in their global con_guration "Stimulus 0 and 1\ or 2 and 3#[ BOTH problems were those in which the two comparison stimuli di}ered in both their global con_guration and local elements "Stimulus 0 and 3\ or 1 and 2#[ Test sessions consisted of 29 trials\ with _ve trials presented for each problem type "BOTH\ GLOBAL\ LOCAL# and visual half!_eld "LVF\ RVF#[ Incorrect trials were presented again within a test session^ thus\ test sessions continued until 4 correct responses were made in each condition[ Each subject received 1 test sessions for a total of 09 correct responses in each condition[ The number of trials was intentionally kept low to minimize the potential e}ect of familiarity on laterality e}ects\ as has been reported in human and animal subjects ð6\ 09\ 07Ł[ Accuracy and response time were the dependent measures[ Accuracy was the average percentage correct for the _rst 4 trials presented for each problem type "BOTH\ GLOBAL and LOCAL# and visual half!_eld "LVF\ RVF#[ Response time was measured\ in milliseconds\ from the o}set of sample stimulus presentation until a collision was detected between the cursor and one of the two comparison stimuli[ For each subject\ response times were averaged across the 4 correct responses within a test session[ All correct responses were followed by the delivery of food reinforcement "grape juice or peanuts# while incorrect responses were not[ A 2!sec inter!trial!interval sep! arated each trial[ Six chimpanzees preferred to use their right hand to manipulate the joystick and one preferred to use his left hand[
Mean response time (msec)
W[ D[ Hopkins:GlobalÐlocal processing and laterality images
Test session 1 Test session 2
280 210 140 70 0 -70 -140 -210 -280 -350
Local
Global
Both
Problem type
Fig[ 2[ Mean di}erence scores for each problem type and test session[ Positive values re~ect a RVF advantage and negative values re~ect a LVF advantage[
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no visual advantage was found for the GLOBAL prob! lems while a strong LVF advantage was found during test session 1[ Post!hoc analysis using Tukey|s HSD indi! cated a signi_cant di}erence in the di}erence scores between LOCAL and GLOBAL problems for test session 1[ For the BOTH problem\ a LVF advantage was observed during test session 0 and a RVF advantage was observed during test session 1[ To assess individual di}erences in performance and the relation between accuracy and response time\ several correlations were performed[ Speci_cally\ using the di}erence scores for each test session as an independent observation\ correlations between mean accuracy and response time were performed using a Pearson Product Moment correlation[ For the LOCAL\ GLOBAL\ and BOTH problems\ the correlations were 9[01\ −9[94 and −9[07\ respectively[ None of these correlations were sig! ni_cant indicating no speedÐaccuracy tradeo} in hemi! spheric di}erences in performance[ In addition\ for each subject and test session\ the magnitude in visual _eld di}erences for the response time and accuracy data were ranked for each problem type[ Subsequent Spearman Rank Order correlations between each problem type indi! cated a signi_cant negative correlation between LOCAL and GLOBAL problems for the response time data "r −9[60\ P³9[90#[ None of the remaining correlations were signi_cant[
Discussion Three major _ndings emerged from this experiment[ First\ response times to LOCAL discrimination problems were faster when presented to the RVF contrasted with LVF[ Second\ the magnitude in di}erences between visual _eld as a function of the type of discrimination problem increased with repeated testing[ Third\ individual di}er! ences in hemispheric specialization were stable and indi! cated that subjects with largest magnitude in asymmetry for LOCAL problems similarly had large visual _eld di}erence in the opposite direction for GLOBAL prob! lems[ In many respects\ the overall RVF advantage in pro! cessing LOCAL problems are comparable to those reported in human subjects using similar\ if not identical types of visual stimuli ð29Ł[ In humans\ the RVF advan! tage for LOCAL problems has been more frequently reported than the LVF advantage in processing GLO! BAL problems and the visual _eld advantage for the chimpanzees was more robust for the LOCAL problems[ Based on these cumulative data\ I would argue that com! parable neural structures are involved in the lateralized processing of hierarchical visual stimuli in humans and chimpanzees[ Horel ð04Ł has found in monkeys that the dorsal half of the inferotemporal cortex is critical in per! forming LOCAL discriminations comprised from hier! archical compound stimuli[ Similar evidence has been reported in humans with selective lesions in this area ð8Ł
but the human _ndings are constrained by the hemisphere which is lesioned "primarily the left#[ Comparable lesion data are not available in monkeys and this warrants fur! ther investigation[ The RVF advantage for LOCAL problems in the chim! panzees di}er from those reported in humans and baboons by Fagot and Deruelle ð7Ł[ In the only other experiment investigating laterality and global:local dis! crimination in nonhuman primates\ Fagot and Deruelle ð7Ł examined laterality in global and local processing and found a slight but signi_cant LVF advantage in pro! cessing stimuli that di}ered in their global con_guration[ Some of the di}erences in _ndings may be procedural as Fagot and Deruelle ð7Ł tested their baboons by presenting blocks of a particular set of discrimination problems[ By contrast\ in this study\ GLOBAL and LOCAL problems were intermixed within a test session[ Further inves! tigations are needed to resolve this issue[ The accuracy data were not extremely high in this study but it was not expected to be in light of the fact that the apes had not been exposed to 099 msec presentation durations with these types of stimuli[ Notwithstanding\ it is unlikely that the chimpanzees| relative poor per! formance can account for the observed visual _eld di}er! ences in response time because these data were based on an equal number of correct responses in each test condition[ If the incorrect responses had not been re! administered within a test session\ then it might have compromised the interpretation of the laterality e}ects in response time because of speedÐaccuracy tradeo}s[ The use of a balanced design\ in terms of the collection of response time data\ precludes this explanation[ More! over\ there were individual di}erences in overall accuracy but all seven chimpanzees exhibited a RVF advantage in response time for the LOCAL problems[ In fact\ com! bining the data from both sessions\ the chimpanzees showed a RVF advantage for LOCAL processing in 02 of the possible 03 conditions "6 apes×1 test sessions#[ For the GLOBAL problems\ a LVF advantage was observed in 7 of the 03 conditions[ This consistency in performance would not be predicted had accuracy in~u! enced the distribution of response times[ The overall response times for LOCAL\ GLOBAL and BOTH problems were 0967\ 897\ and 839 msec\ respec! tively[ These data are consistent with our previous studies demonstrating a global!to!local precedence in the pro! cessing of hierarchical visual stimuli in chimpanzees ð10Ł[ However\ in our previous studies\ a 499 msec presentation duration was employed while in this study\ a 099 msec presentation was used[ Thus\ the results from this study can be interpreted as a replication of previous _ndings but using a faster stimulus presentation duration[ One limitation of this study was the use of only one stimulus presentation duration resulting in unilateral pro! jection of the sample stimulus[ Sample stimulus pres! entation is an important factor in the assessment of laterality ð18Ł and this could be particularly important for stimuli requiring di}erent levels of processing such as
W[ D[ Hopkins:GlobalÐlocal processing and laterality images
global:local stimuli[ Other limitations include the use of only one set of stimuli and the relatively small number of subjects\ particularly females[ Nevertheless\ none of these limitations negate the signi_cance of the _ndings but only limit the degree of generality[ In conclusion\ the evidence of lateralized processing of visual stimuli di}ering on the basis of global and local features in chimpanzees serves as further evidence of hemispheric specialization in animals[ The _ndings fur! ther suggest homologous processes in the manifestation of laterality in chimpanzees and humans[ The extent to which di}erent species similarly manifest asymmetries in global:local processing should be investigated in future studies as a means to establish the evolutionary basis of this function[
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Acknowled`ements*Funding for this research was provided by NIH grants RR!99054 and NS!18463 to the Yerkes Regional Primate Research Center of Emory University[ The Yerkes Primate Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care[ The American Psychological Associations guideline for the ethical treatment of animals was fully adhered to during all phases of this study[
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References 08[ 0[ Bard\ K[ A[ Evolutionary foundations of intuitive parenting[ A special case of maternal competence in chimpanzees[ Early Development and Parentin` 2\ 08Ð17\ 0883[ 1[ Bradshaw\ J[ and Rogers\ L[ J[ The Evolution of Lat! eral Asymmetries\ Lan`ua`e\ Tool Use\ and Intellect[ Academic Press\ San Diego\ CA\ 0882[ 2[ Corballis\ M[ C[ The Lopsided Ape] Evolution of the Generative Mind[ Oxford University Press\ New York\ 0881[ 3[ Delis\ D[ C[\ Robertson\ L[ C[ and Efron\ R[ Hemi! spheric specialization of memory for visual hier! archical stimuli[ Neuropsycholo`ia 13\ 194Ð103\ 0875[ 4[ Ettlinger\ G[ Hand preference\ ability\ and hemi! spheric specialization] How far are these factors related in the monkey< Cortex 13\ 278Ð287\ 0877[ 5[ Fagot\ J[ and Vauclair\ J[ Manual laterality in non! human primates] A distinction between handedness and manual specialization[ Psycholo`ical Bulletin 098\ 65Ð78\ 0880[ 6[ Fagot\ J[ and Vauclair\ J[ Video!task assessment of stimulus novelty e}ects on hemispheric lateralization in baboons "Papio papio#[ Journal of Comparative Psycholo`y 097\ 045Ð052\ 0883[ 7[ Fagot\ J[ and Deruelle\ C[ Processing of global and local visual information and hemispheric spe! cialization in humans "Homo sapiens# and baboons "Papio papio#[ Journal of Experimental Psycholo`y] Human Perception and Performance\ in press[ 8[ Farah\ M[ J[ Visual A`nosia[ MIT Press\ Cambridge\ 0889[ 09[ Goldberg\ E[ and Costa\ L[ Hemisphere di}erences
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macaques "Macaca fuscata#[ Science 191\ 213Ð216\ 0867[ Sergent\ J[ The cerebral balance of power] Con! frontation or cooperation< Journal of Experimental Psycholo`y] Human Perception and Performance 7\ 142Ð161\ 0871[ Sergent\ J[ and Hellige\ J[ B[ Role of input factors in visual!_eld asymmetries[ Brain and Co`nition 4\ 063Ð 088\ 0875[ Van Kleek\ M[ H[ Hemispheric di}erences in global versus local processing of hierarchical visual stimuli by normal subjects] New data and a meta!analysis of previous studies[ Neuropsycholo`ia 16\ 0054Ð0067\ 0878[ Vauclair\ J[\ Fagot\ J[ and Hopkins\ W[ D[ Rotation of mental images in baboons when visual input is directed to the left cerebral hemisphere[ Psycho! lo`ical Science 3\ 88Ð092\ 0882[ Ward\ J[ P[ and Hopkins\ W[ D[ "Editors# Primate
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Laterality] Current Behavioral Evidence of Primate Asymmetries[ Springer!Verlag\ New York\ 0882[[ Washburn\ D[ A[\ Hopkins\ W[ D[ and Rumbaugh\ D[ M[ Video!task assessment of learning] The e}ects of stimulus movement[ Journal of Experimental Psy! cholo`y] Animal Behavior Processes 04\ 282Ð399\ 0878[ Washburn\ D[ A[ and Rumbaugh\ D[ M[ Testing primates with joystick!based automated apparatus] Lessons from the Language Research Center|s Com! puterized Test System[ Behavior Research Methods\ Instruments and Computers 13\ 046Ð053\ 0881[ Warren\ J[ M[ Handedness and laterality in humans and other animals[ Physiolo`ical Psycholo`y 7\ 240Ð 248\ 0879[ Wilde\ J[\ Vauclair\ J[ and Fagot\ J[ Eye movements in baboons performing a matching!to!sample task presented within a divided!_eld format[ Behavioural Brain Research 22\ 50Ð69\ 0883[
Pergamon
Neuropsycholo`ia\ Vol[ 24\ No[ 2\ pp[ 232Ð237\ 0886 Þ 0886 Elsevier Science Ltd[ All rights reserved Printed in Great Britain 9917Ð2821:86 ,06[99¦9[99
PII] S9917Ð2821"85#99978Ð8
Hemispheric specialization for local and global processing of hierarchical visual stimuli in chimpanzees "Pan troglodytes# WILLIAM D[ HOPKINS Department of Psychology\ Berry College\ P[O[ Box 384908\ Mount Berry\ GA 29038!4918\ U[S[A[ "Received 1 April 0885^ accepted 11 July 0885#
Abstract*This study examined laterality in global and local processing of hierarchical compound stimuli in seven chimpanzees "Pan tro`lodytes#[ A divided visual half!_eld paradigm was used that allowed for unilateral presentation of compound stimuli to either the left or right hemisphere[ Comparison stimuli di}ering on the basis of their global con_guration\ local elements or both features followed sample stimulus presentation[ Subjects were required to accurately discriminate the comparison stimuli on the basis of these features relative to the sample stimulus[ No laterality e}ects were found for accuracy^ however\ for reaction time\ a signi_cant interaction was found between visual _eld and processing mode[ An overall right visual _eld advantage was found for local processing but no visual _eld di}erences for global processing[ The overall results are consistent with previous _ndings in humans and suggests homologous lateralization in chimpanzees and humans[ Þ 0886 Elsevier Science Ltd[ All rights reserved[ Key Words] global:local processing^ hierarchical compound stimuli^ chimpanzee[
tachistoscopically presented hierarchical compound stimuli unilaterally and compared performance between hemispheres when subjects are required to respond on the basis of the global con_guration or local elements of the stimulus[ Hierarchical compound stimuli are typically larger stimuli comprised of smaller elements that are either identical or di}erent in appearance from the shape of the larger stimulus[ An example of four hierarchical stimuli is depicted in Fig[ 0[ As can be seen\ the larger Arabic letters {H| and {L| can be constructed from the smaller letters[ Some have suggested that the right hemisphere is superior in pro! cessing global aspects of hierarchical compound stimuli while the left hemisphere is superior in processing local elements and there is empirical evidence to support this dichotomy ð13\ 17\ 29Ł[ For example\ in human intact subjects\ Martin ð13Ł presented hierarchical stimuli to either the left or right visual half!_eld and required sub!
Introduction Recent studies clearly suggest the presence of hemispheric specialization in nonhuman species ð0\ 21Ł[ For example\ in nonhuman primates\ there is evidence of population! level hand preferences ð5\ 05\ 12\ 14\ 21Ł\ asymmetries in visualÐspatial processing\ perception and production of facial expressions ð00\ 02\ 06\ 15\ 20Ł and in cognitive functions ð01\ 03\ 08\ 16Ł[ These cumulative results seri! ously challenge the long held belief that hemispheric spe! cialization is unique to humans ð2\ 4\ 24Ł[ A fundamental theoretical and empirical question that remains is whether the asymmetries observed in animals are hom! ologous to those observed in humans or whether they represent species!speci_c adaptations[ One way in which the human left and right hemispheres have been dichotomized has been in their propensity to process stimuli that di}er on the basis of either their global con_guration or local elements[ To assess this model of hemispheric specialization\ investigators have
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Address for correspondance] Department of Psychology\ Berry College\ P[O[ Box 384908\ Mount Berry\ GA 29038!4918\ U[S[A[ "Also at Yerkes Regional Primate Research Center\ Emory University\ Emory University\ Atlanta\ GA 29211\ U[S[A[#
L L L L L LLL L L L L
H H H H HHHH
H H H H H HH H H H H H
(1) (2) (3) (4) Fig[ 0[ Stimuli used in the experiment[
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jects to report the local elements or global con_guration of the sample stimulus[ Subjects showed a right visual _eld advantage in reaction time when required to report the local elements of the stimulus[ No visual _eld di}er! ences were found in processing the global attributes of the stimuli[ Clinical studies support the dichotomy in hemispheric specialization and global:local discrimi! nation[ For example\ Delis et al[ ð3Ł asked patients with right and left hemisphere lesions to draw hierarchical compound stimuli[ Patients with right hemisphere lesions tended to draw the global aspects of the stimulus while patients with left hemisphere lesions tended to draw the local elements of the stimulus[ From a comparative perspective\ very little is known about the processing of hierarchial compound stimuli[ Recently\ Hopkins and Washburn ð10Ł have reported that chimpanzees exhibit a global!to!local precedence in the processing of hierarchical compound stimuli while rhesus monkeys do not[ Global!to!local precedence refers to performance in which subjects respond more quickly or more accurately to global aspects of compound stimuli compared to their local features[ Fagot and Deruelle ð7Ł reported the lack of a global!to!local precedence in the processing of hierarchical compound stimuli in a sample of 7 baboons while human subjects tested with the same stimuli did show the precedence[ Notwithstanding the lack of global!to!local precedence in baboons\ the baboons did discriminate stimuli that di}ered on the basis of their global con_guration when presented to the left visual!_eld\ suggesting a right hemisphere advantage[ No hemispheric advantages were reported in the processing of local aspects of these hierarchical stimuli[ The focus in this study was to determine whether the left and right cerebral hemispheres of chimpanzees di}erentially process hierarchical compound stimuli that di}er on the basis of their global con_guration\ local features or both attributes[ Based on _ndings by Martin ð13Ł in human subjects and those reported by Fagot and Deruelle ð7Ł\ I hypothesized that chimpanzees would dem! onstrate a right visual _eld advantage in processing the local elements of a hierarchical compound stimulus and a left visual _eld advantage when processing the global aspects of hierarchical compound stimuli[ For hier! archical stimuli di}ering on both global and local cues\ no visual _eld di}erences were predicted because subjects could utilize either cue to respond correctly on a given trial[
Methods Subjects Seven chimpanzees "Pan tro`lodytes#\ including _ve males and two females\ ranging from 6 to 09 years of age served as subjects[ All seven chimpanzees were raised in captivity at the Yerkes Regional Primate Research Center following standard nursery protocol for great apes ð0Ł[
Apparatus The basic test system used is referred to as the Language Research Center Computerized Test System "LRC!CTS# and has been described in detail elsewhere ð23Ł[ Each test system consisted of a personal computer "275!compatible#\ a 02!in[ color monitor\ and an analog joystick[ Food reinforcement was delivered by the experimenter by handing the food through the cage to the chimpanzee[
Stimuli The stimuli used are depicted in Fig[ 0 and are one set of stimuli that have been previously employed in our comparative visual perception studies of hierarchical compound stimuli in monkeys and chimpanzees ð10Ł[ The larger stimuli were 2[64 cm×1[4 cm in dimension[ The individual element features were 5 mm×5 mm with 0 mm spaces separating individual fea! ture within a larger stimulus[ The stimuli were white and pro! jected on the black background of the computer monitor[
Divided visual _eld task Prior to the onset of testing\ all subjects were trained to reliably use the joystick test system and perform a number of cognitive tasks including simultaneous and sequential matching! to!sample ð11\ 22Ł[ In this study\ a sequential matching!to!sam! ple paradigm presented within a divided visual!_eld "DVF# format was employed[ Use of the DVF testing format allowed for unilateral presentation of visual stimuli and therefore assess! ment of hemispheric specialization in neurologically intact sub! jects[ The general DVF testing procedure has been described in detail elsewhere ð07\ 19Ł[ At the beginning of each trial\ a cursor "a {¦| sign\ 8 mm×8 mm# and a _xation point "0 cm in diam! eter# appeared on the computer monitor[ The _xation point was positioned in the center of the computer monitor while the cursor was randomly positioned on the screen[ In order to view the screen\ subjects had to look through a viewport that separated the monitor from the cage[ The viewport was metal\ 49 cm in length and shaped like a rectangular funnel[ The wide end of the viewport was 26 cm×15 cm and _tted squarely over the computer monitor[ The narrow end of the viewport was 04 cm×5 cm with two eye holes cut equidistant from each other[ The eye holes were 1[4 cm in diameter[ The chimpanzees had to look through the eye holes to see the computer monitor[ The viewport allowed for control of the distance that each subject maintained from the _xation point each trial\ a necessary con! dition for assurance of unilateral presentation[
Procedure Each trial\ subjects were required to move their cursor to the _xation point displayed in the center of the computer monitor[ If this condition was met\ then a sample stimulus was presented for 099 msec either to the left or right side of the _xation point[ A 099 msec presentation duration precluded bilateral overlap in stimulus presentation due to saccadic eye movements ð25Ł[ The sample stimulus was one of the four stimuli displayed in Fig[ 0[ The inside edge of the sample stimulus was laterally placed at a visual angle of 5 degrees from the _xation point[ After sample stimulus presentation\ the sample stimulus was erased from the monitor and two comparison stimuli appeared equidistant from the _xation point[ One comparison stimulus was 4 cm above the _xation point and one was 4 cm below the _xation point[ The positive comparison stimulus was identical
Results The accuracy and response time data were analyzed using a complete within!subjects analysis of variance "ANOVA#[ Test session ð0\ 1Ł\ visual half!_eld "LVF\ RVF# and problem type "GLOBAL\ LOCAL\ BOTH# were the independent variables of interest[ A priori plan! ned comparisons in performance between the LVF and RVF for each problem were speci_ed in the ANOVA model[ Overall\ no signi_cant main e}ects or interactions were found for the accuracy data[ The mean percentage correct for the LOCAL\ GLOBAL and BOTH problems were 54)\ 40) and 45)\ respectively[ For the response time data\ signi_cant main e}ects for visual half!_eld ðF"0\5# 6[43\ P³9[93Ł and problem ðF"1\01# 4[08\ P³9[93Ł were found[ A signi_cant two!way interaction was found between visual half!_eld and problem ðF"1\01# 3[03\ P³9[94Ł and a signi_cant three!way interaction was found between test session\ problem and visual half!_eld ðF"1\01# 3[44\ P³9[93Ł[ Depicted in Fig[ 1 are the mean response times for each visual half! _eld and problem type[ The a priori contrasts indicated
1300 1250 1200 1150 1100 1050 1000 950 900 850 800 750 700
234
Local Global Both
LVF
RVF
Visual half-field
Fig[ 1[ Mean response times as a function of problem type and visual half!_eld[
a signi_cant di}erence in response between the LVF and RVF for the LOCAL problems ðt"5# 3[09\ P³9[995Ł[ No overall visual half!_eld di}erences were found for the GLOBAL and BOTH problems[ These _ndings account for the signi_cant interaction found between problem type and visual half!_eld[ With respect to the three!way interaction between test session\ visual half!_eld and problem type\ the data were transformed to simplify the interpretation of this result[ For each subject\ the mean response for the LVF was subtracted from the mean response time for the RVF within a test session and between problem types[ This resulted in either negative and positive di}erence scores with positive values re~ecting a RVF advantage and negative values re~ecting a LVF advantage[ Values on or about zero would re~ect either a slight or no visual _eld advantage[ The di}erence scores were subjected to a within!subject design ANOVA with test session and problem type as the independent variables[ A signi_cant two!way interaction was found between test session and problem type ðF"1\01# 3[44\ P³9[93Ł[ The mean di}er! ence score for each problem type and test session can be seen in Fig[ 2[ For the LOCAL problems\ a consistent RVF advantage was found between test sessions 0 and 1\ although the magnitude of this e}ect increased from session 0 to 1[ In contrast\ within test session 0\ essentially 350
Difference score (RVF-LVF)
to the sample stimulus while the alternative stimulus was a foil[ The foil stimulus was always one of the remaining three stimuli comprising the stimulus library[ A correct response was rec! orded when subjects moved their cursor to the positive com! parison stimulus[ Incorrect responses were recorded when the subjects moved their cursor to the foil[ Based on which com! parison stimuli were displayed\ there were three possible types of perceptual discrimination problems that could occur on a given trial[ LOCAL problems were those in which the two comparison stimuli di}ered in their local elements "Stimulus 0 and 2\ or 1 and 3#[ GLOBAL problems were those in which the two comparison stimuli di}ered in their global con_guration "Stimulus 0 and 1\ or 2 and 3#[ BOTH problems were those in which the two comparison stimuli di}ered in both their global con_guration and local elements "Stimulus 0 and 3\ or 1 and 2#[ Test sessions consisted of 29 trials\ with _ve trials presented for each problem type "BOTH\ GLOBAL\ LOCAL# and visual half!_eld "LVF\ RVF#[ Incorrect trials were presented again within a test session^ thus\ test sessions continued until 4 correct responses were made in each condition[ Each subject received 1 test sessions for a total of 09 correct responses in each condition[ The number of trials was intentionally kept low to minimize the potential e}ect of familiarity on laterality e}ects\ as has been reported in human and animal subjects ð6\ 09\ 07Ł[ Accuracy and response time were the dependent measures[ Accuracy was the average percentage correct for the _rst 4 trials presented for each problem type "BOTH\ GLOBAL and LOCAL# and visual half!_eld "LVF\ RVF#[ Response time was measured\ in milliseconds\ from the o}set of sample stimulus presentation until a collision was detected between the cursor and one of the two comparison stimuli[ For each subject\ response times were averaged across the 4 correct responses within a test session[ All correct responses were followed by the delivery of food reinforcement "grape juice or peanuts# while incorrect responses were not[ A 2!sec inter!trial!interval sep! arated each trial[ Six chimpanzees preferred to use their right hand to manipulate the joystick and one preferred to use his left hand[
Mean response time (msec)
W[ D[ Hopkins:GlobalÐlocal processing and laterality images
Test session 1 Test session 2
280 210 140 70 0 -70 -140 -210 -280 -350
Local
Global
Both
Problem type
Fig[ 2[ Mean di}erence scores for each problem type and test session[ Positive values re~ect a RVF advantage and negative values re~ect a LVF advantage[
235
W[ D[ Hopkins:GlobalÐlocal processing and laterality images
no visual advantage was found for the GLOBAL prob! lems while a strong LVF advantage was found during test session 1[ Post!hoc analysis using Tukey|s HSD indi! cated a signi_cant di}erence in the di}erence scores between LOCAL and GLOBAL problems for test session 1[ For the BOTH problem\ a LVF advantage was observed during test session 0 and a RVF advantage was observed during test session 1[ To assess individual di}erences in performance and the relation between accuracy and response time\ several correlations were performed[ Speci_cally\ using the di}erence scores for each test session as an independent observation\ correlations between mean accuracy and response time were performed using a Pearson Product Moment correlation[ For the LOCAL\ GLOBAL\ and BOTH problems\ the correlations were 9[01\ −9[94 and −9[07\ respectively[ None of these correlations were sig! ni_cant indicating no speedÐaccuracy tradeo} in hemi! spheric di}erences in performance[ In addition\ for each subject and test session\ the magnitude in visual _eld di}erences for the response time and accuracy data were ranked for each problem type[ Subsequent Spearman Rank Order correlations between each problem type indi! cated a signi_cant negative correlation between LOCAL and GLOBAL problems for the response time data "r −9[60\ P³9[90#[ None of the remaining correlations were signi_cant[
Discussion Three major _ndings emerged from this experiment[ First\ response times to LOCAL discrimination problems were faster when presented to the RVF contrasted with LVF[ Second\ the magnitude in di}erences between visual _eld as a function of the type of discrimination problem increased with repeated testing[ Third\ individual di}er! ences in hemispheric specialization were stable and indi! cated that subjects with largest magnitude in asymmetry for LOCAL problems similarly had large visual _eld di}erence in the opposite direction for GLOBAL prob! lems[ In many respects\ the overall RVF advantage in pro! cessing LOCAL problems are comparable to those reported in human subjects using similar\ if not identical types of visual stimuli ð29Ł[ In humans\ the RVF advan! tage for LOCAL problems has been more frequently reported than the LVF advantage in processing GLO! BAL problems and the visual _eld advantage for the chimpanzees was more robust for the LOCAL problems[ Based on these cumulative data\ I would argue that com! parable neural structures are involved in the lateralized processing of hierarchical visual stimuli in humans and chimpanzees[ Horel ð04Ł has found in monkeys that the dorsal half of the inferotemporal cortex is critical in per! forming LOCAL discriminations comprised from hier! archical compound stimuli[ Similar evidence has been reported in humans with selective lesions in this area ð8Ł
but the human _ndings are constrained by the hemisphere which is lesioned "primarily the left#[ Comparable lesion data are not available in monkeys and this warrants fur! ther investigation[ The RVF advantage for LOCAL problems in the chim! panzees di}er from those reported in humans and baboons by Fagot and Deruelle ð7Ł[ In the only other experiment investigating laterality and global:local dis! crimination in nonhuman primates\ Fagot and Deruelle ð7Ł examined laterality in global and local processing and found a slight but signi_cant LVF advantage in pro! cessing stimuli that di}ered in their global con_guration[ Some of the di}erences in _ndings may be procedural as Fagot and Deruelle ð7Ł tested their baboons by presenting blocks of a particular set of discrimination problems[ By contrast\ in this study\ GLOBAL and LOCAL problems were intermixed within a test session[ Further inves! tigations are needed to resolve this issue[ The accuracy data were not extremely high in this study but it was not expected to be in light of the fact that the apes had not been exposed to 099 msec presentation durations with these types of stimuli[ Notwithstanding\ it is unlikely that the chimpanzees| relative poor per! formance can account for the observed visual _eld di}er! ences in response time because these data were based on an equal number of correct responses in each test condition[ If the incorrect responses had not been re! administered within a test session\ then it might have compromised the interpretation of the laterality e}ects in response time because of speedÐaccuracy tradeo}s[ The use of a balanced design\ in terms of the collection of response time data\ precludes this explanation[ More! over\ there were individual di}erences in overall accuracy but all seven chimpanzees exhibited a RVF advantage in response time for the LOCAL problems[ In fact\ com! bining the data from both sessions\ the chimpanzees showed a RVF advantage for LOCAL processing in 02 of the possible 03 conditions "6 apes×1 test sessions#[ For the GLOBAL problems\ a LVF advantage was observed in 7 of the 03 conditions[ This consistency in performance would not be predicted had accuracy in~u! enced the distribution of response times[ The overall response times for LOCAL\ GLOBAL and BOTH problems were 0967\ 897\ and 839 msec\ respec! tively[ These data are consistent with our previous studies demonstrating a global!to!local precedence in the pro! cessing of hierarchical visual stimuli in chimpanzees ð10Ł[ However\ in our previous studies\ a 499 msec presentation duration was employed while in this study\ a 099 msec presentation was used[ Thus\ the results from this study can be interpreted as a replication of previous _ndings but using a faster stimulus presentation duration[ One limitation of this study was the use of only one stimulus presentation duration resulting in unilateral pro! jection of the sample stimulus[ Sample stimulus pres! entation is an important factor in the assessment of laterality ð18Ł and this could be particularly important for stimuli requiring di}erent levels of processing such as
W[ D[ Hopkins:GlobalÐlocal processing and laterality images
global:local stimuli[ Other limitations include the use of only one set of stimuli and the relatively small number of subjects\ particularly females[ Nevertheless\ none of these limitations negate the signi_cance of the _ndings but only limit the degree of generality[ In conclusion\ the evidence of lateralized processing of visual stimuli di}ering on the basis of global and local features in chimpanzees serves as further evidence of hemispheric specialization in animals[ The _ndings fur! ther suggest homologous processes in the manifestation of laterality in chimpanzees and humans[ The extent to which di}erent species similarly manifest asymmetries in global:local processing should be investigated in future studies as a means to establish the evolutionary basis of this function[
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Acknowled`ements*Funding for this research was provided by NIH grants RR!99054 and NS!18463 to the Yerkes Regional Primate Research Center of Emory University[ The Yerkes Primate Center is fully accredited by the American Association for Accreditation of Laboratory Animal Care[ The American Psychological Associations guideline for the ethical treatment of animals was fully adhered to during all phases of this study[
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Laterality] Current Behavioral Evidence of Primate Asymmetries[ Springer!Verlag\ New York\ 0882[[ Washburn\ D[ A[\ Hopkins\ W[ D[ and Rumbaugh\ D[ M[ Video!task assessment of learning] The e}ects of stimulus movement[ Journal of Experimental Psy! cholo`y] Animal Behavior Processes 04\ 282Ð399\ 0878[ Washburn\ D[ A[ and Rumbaugh\ D[ M[ Testing primates with joystick!based automated apparatus] Lessons from the Language Research Center|s Com! puterized Test System[ Behavior Research Methods\ Instruments and Computers 13\ 046Ð053\ 0881[ Warren\ J[ M[ Handedness and laterality in humans and other animals[ Physiolo`ical Psycholo`y 7\ 240Ð 248\ 0879[ Wilde\ J[\ Vauclair\ J[ and Fagot\ J[ Eye movements in baboons performing a matching!to!sample task presented within a divided!_eld format[ Behavioural Brain Research 22\ 50Ð69\ 0883[