Age and culture modulate object processing and … · on physical features and categorical...

transcript

Extensivebehavioralstudiessuggestthatinvisualpro-cessing,collectivistexperiencesbiasEastAsianstoat-tendtocontextualinformation,whereasindividualisticexperiencesbiasWesternerstoprocessobjectspreferen-tially(Chua,Boland,&Nisbett,2005;Nisbett&Masuda,2003;Nisbett&Miyamoto,2005;Nisbett,Peng,Choi,&Norenzayan,2001).Theseeffectsofcultureoncognitivefunctionhavebeendemonstratedacrossmanydomains,includingperceptualprocessing,semanticorganization,memory,reasoning,andneuralfunction.Attheperceptuallevel,Chuaetal.(2005)foundthat,whenviewingcom-plexscenes,EastAsiansmademoresaccadestotheback-groundcontexts,whereasWesternersfixatedfasterandlongeroncentralobjects.Instudiesonsemanticorganiza-tion,EastAsianswerefoundtoassociateimagesofpeopleonthebasisoffunctionalrelationships(suchasgroupingtogetheramotherandherchildbecauseofthematernalrelationship),whereasWesternersbasedtheirassociationsonphysicalfeaturesandcategoricalmembership(suchasgroupingtogetherawomanandamanbecausetheywerebothadults)(Chiu,1972;Ji,Zhang,&Nisbett,2004).Inamemorystudy,MasudaandNisbett(2001)demonstrated

thatEastAsianswerelesslikelytorecognizetargetob-jectsthattheyhadpreviouslyencodediftheobjects’back-groundhadchanged,incontrastwithWesterners,whoseobjectmemorywaslessaffectedbybackgroundchanges.Most recently,Gutchess,Welsh,Boduroglu, andPark(2006),usingstimulisimilartothoseusedbyMasudaandNisbett,observedculturaldifferencesintheventralvisualcortexaswellasinareasassociatedwithsemanticprocessingofobjects.Westernerswhoencodedcomplexpicturescontainingacentralobjectagainstabackgroundshowedmoreengagementofbilateralmiddletemporal,rightsuperiortemporal,andleftsuperiorparietalregions(areasimportantforobjectandsemanticprocessing)thanEastAsians.Incontrast,EastAsians,whenprocessingbackgrounds,showedgreaterengagementofleftoccipi-talandfusiformareas,whichareimplicatedinstructural,perceptualanalyses(Joseph&Gathers,2003).

Inthepresentstudy,weusedtheadaptationparadigmdevelopedbyGohetal.(2004)toinvestigatehowculturemightinteractwithagedifferencesinprocessingobjectsandbackgroundsaswellascontextualbindingofob-jectstobackgrounds.InGohetal.’sstudy,youngadults

Age and culture modulate object processing and object–scene binding in the ventral visual area

Joshua o. Goh University of Illinois at Urbana-Champaign, Urbana, Illinois

Michael W. chee, Jiat choW tan, and Vinod VenkatraManCognitive Neuroscience Laboratory, SingHealth, Singapore

andreW hebrank, eric d. leshikar, lucas Jenkins, bradley P. sutton, anGela h. Gutchess, and denise c. Park

University of Illinois at Urbana-Champaign, Urbana, Illinois

Behavioraldifferencesinthevisualprocessingofobjectsandbackgroundsasafunctionofculturalgrouparewelldocumented.Recentneuroimagingevidencealsopointstoculturaldifferencesinneuralactivationpatterns.ComparedwithEastAsians,Westerners’visualprocessingismoreobjectfocused,andtheyactivateneuralstructuresthatreflectthisbiasforobjects.Inarecentadaptationstudy,EastAsianolderadultsshowedanabsenceofanobject-processingareabutnormaladaptationforbackgroundareas.Inthepresentstudy,75youngandoldadults(halfEastAsianandhalfWestern)weretestedinanfMR-adaptationstudytoexaminedifferencesinobjectandbackgroundprocessingaswellasobject–backgroundbinding.Wefoundequivalentbackgroundprocessingintheparahippocampalgyrusinallfourgroups,diminishedbindingprocessesinthehippocampusinelderlyEastAsiansandWesterners,anddiminishedobjectprocessinginelderlyversusyoungadultsinthelateraloccipitalcomplex.Moreover,elderlyEastAsiansshowedsignificantlylessadaptationresponseintheobjectareasthandidelderlyWesterners.Thesefindingsdemonstratethemalleabilityofperceptualprocessesasaresultofdifferencesincohort-specificexperiencesorinculturalexposureovertime.

Cognitive, Affective, & Behavioral Neuroscience2007, 7 (1), 44-52

D. C. Park, denisep@uiuc.edu

Culture, Age, And VisuAl ProCessing 45

werepresentedwithquartetsofpicturesinwhicheitherthecentralobjectorthebackgroundofthepicturevaried(Figure1),andtheattenuationofthebloodoxygenleveldependent(BOLD)signalthatoccurreduponrepetitionofelementsofthepictureswasmeasured(seeGrill-Spector&Malach,2001).Inconditionsinwhichtheobjectwasre-peatedandthebackgroundchanged,theBOLDresponsediminished,relativetowhenboththeobjectandtheback-groundwerechanged, in the lateraloccipitalcomplex

(LOC)inbothhemispheres(Grill-Spector,Kourtzi,&Kanwisher,2001;Malachetal.,1995).Thissuggeststhattheseareaswereengagedforprocessingobjectsandthattheyshowedanadaptedresponseastheobjectsrepeatedacrossthequartets.Similarly,whentheobjectchangedandthebackgroundwasheldconstant,bilateralparahip-pocampalplaceareas(PPA)showedadaptation,suggest-ingthattheseareaswerespecializedforbackgroundpro-cessing(Epstein,Graham,&Downing,2003;Epstein&

P1 P2 P3 P4

+ + + + +

SD IPI SD IPI SD SDIPI

Quartet

+ + + + +

IQI IQI IQI

Figure 1. Hybrid block/event-related fMRI experiment consisting of quartets of picture stimuli. (A) The four quartet conditions: four repeated objects and scenes (OO: old object, old scene); four novel scenes with a repeated object (ON: old object, new scene); four novel objects within a repeated scene (NO: new object, old scene); and four novel objects with four novel scenes (NN: new object, new scene). (B) Picture stimulus duration (SD) was 1.5 sec, with an interpicture interval (IPI) of 250 msec and mean interquartet interval (IQI) of 9 sec. A fixation cross was shown during the inter-vals when no picture was displayed.

46 goh et Al.

Kanwisher,1998).Finally,Henke,Weber,Kneifel,Wie-ser,andBuck(1999)demonstratedthatbindingareasinbilateralparahippocampalgyrus(separatefromthePPA)andrighthippocampusshowedadaptationwhenbothele-mentswererepeatedbutnotwhenbothwerevaried,sug-gestingthattheseareaswereimportantforcontextuallybindingatargetobjecttoascene;thiswasthefirststudythat showedbinding-relatedprocessingwhensubjectspassivelyviewedscenesratherthanwhentheyactivelyattemptedtobindsceneelements.

Agingisconsistentlyassociatedwithpoorerepisodicmemoryrelatedtobindingdeficitsatencoding(Chalfonte&Johnson,1996;Mitchell,Johnson,Raye,&D’Esposito,2000;Mitchell,Johnson,Raye,Mather,&D’Esposito,2000;Naveh-Benjamin,Hussain,Guez,&Bar-On,2003;Park,Puglisi,&Sovacool,1984;Spencer&Raz,1995).Cheeetal.(2006)testedasampleofolderadultsusingtheGohetal. (2004)paradigmto investigate theneu-ralcorrelatesofthesebindingdeficitscharacteristicofaging.WhencomparedwiththedatafromyoungadultsinGohetal.’sstudy,thedatafromtheCheeetal.studyshowedgreatlyreducedbindingactivityinolderadultsinthemedialtemporalregionsand,surprisingly,thetotalabsenceofobjectprocessingadaptationintheLOC.Incontrast,thebackgroundprocessingareasintheparahip-pocampalregionsshowedsimilarmagnitudesofadapta-tionresponsesforoldandyoungadults.Infollow-upex-periments,objectprocessingadaptationintheLOCwasdemonstratedagainwhenolderadultswereinstructedtoattendtothecentralobjectinthescene,aswellaswhentheolderadultsviewedtheobjectalonewithoutaback-ground.ThusthenonrecruitmentoftheLOCwhentheolderadultspassivelyviewedcomplexpicturesappearstorepresentaperceptualbiasdrivenbyage-relatedchangesinvisualattention(Madden&Langley,2003;Maylor&Lavie,1998;McCarley,Mounts,&Kramer,2004;Milhametal.,2002;Pringle,Irwin,Kramer,&Atchley,2001).

It isnoteworthy that thesubjects inbothGohetal.(2004)andCheeetal.(2006)wereSingaporeansofChi-neseheritage.BothbehavioralandimagingdatasuggestabiasinWesternerstoprocessobjectswithintheback-ground,whichraisesthequestionofwhetherthelossofobjectsensitivityinolderChineseadultsreflectsacultur-allybiasedvisualperceptualprocessinginEastAsiansthatisexacerbatedbychangesinvisualattentionwithage.

Toevaluatetheneuralcorrelatesofculturaldifferencesinperceptualprocessingasafunctionofage,wetested38youngandelderlyWesternsubjects(notofAsiandescent)usingtheGohetal.(2004)paradigmandcontrastedthedatafromthesesubjectswiththedatafromtheyoungandelderlyEastAsianswhoparticipatedintheGohetal.andCheeetal.(2006)studies.Wehypothesizedthatduetoprolongedexperiencewithinanobject-biasedculture,elderlyWesternerswouldshowgreaterengagementofobject-processingareasthandidtheelderlyEastAsiansfromtheCheeetal.study.Specifically,weexpectedtheelderlyWesternerstoshowgreaterobject-processingac-tivityinthelateraloccipitalareasthantheelderlyEastAsians.Wealsopredicted,onthebasisofbehavioralfind-ingsofcross-culturaldifferences,thatolderWesterners

wouldshowlessactivityinthebackgroundprocessingareasthanolderEastAsians.Finally,withregardtotheex-tensiveliteraturedocumentingbehavioralandfunctionaldeficitsinbindingwithageinWesterners,weexpectedbothelderlyEastAsiansandelderlyWesternerstoshowdeficitsinbindingreflectedbyreducedbinding-relatedactivity,relativetoyoungadults,inthehippocampalandparahippocampalregions.

MeTHOD

SubjectsThirty-eightright-handedvolunteers,including19youngWest-

erners(12malesand7femalesranginginagefrom19to27withameanageof21.7years)and19elderlyWesterners(14femalesand5males,ranginginagefrom60to78withameanageof68.1years)fromtheUnitedStates,gaveinformedconsenttoparticipateinthisstudy.SubjectswerescreenedforsignificantillnessesandcontraindicationsforfMRIscanning.DatafromourpreviousstudyofSingaporeansubjectswereincludedforcomparisonacrosscul-tures.Thesesubjectsincluded20youngEastAsians(13femalesand7malesranginginagefrom20to24withameanageof21.3years)and17elderlyEastAsians(11femalesand6malesranginginagefrom60to75withameanageof66.7years).Allsubjectshadnormalvisionorvisioncorrectedtotheacuityof20/30ontheSnellenchart.Subjectsunderwentneuropsychologicaltesting(seeTable1),andtheyalsotooktheWAIS–RComprehensiontest,whichisaculturallyappropriatemeasureofverbalintelligencewithdiffer-entversionsforEastAsiansandWesterners(Gong,1983;Wechsler,1981).Therewerenosignificantdifferencesacrossage[F(1,69)50.003,n.s.]orculture[F(1,69)50.032,n.s.]insubjects’perfor-manceonthistest,indicatingthatsubjectswerecomparableinthismeasureofgeneralintelligence.

Therewere,however,significanteffectsofageinseveraltestsinvolvingspeedofprocessingandworkingmemory;thisresultisconsistentwiththenotionthatagingisassociatedwithslowing(Madden&Langley,2003;Salthouse,1996). Incontrast, therewasnoeffectofcultureonperformanceinthesespeededworkingmemorytests.TherewasaneffectofageontheMini-MentalStateExam(MMSE)[F(1,69)511.34,p,.01],butthemeanscoreswerestillwellwithinthepopulationnormforelderlysubjects,withalloftheoldersubjectsscoring27orgreater(Crum,Anthony,Bas-sett,&Folstein,1993).ItisimportanttonotethattheMMSEscoresdidnotdifferacrossculturesbetweensubjectswithinthesameagegroup.Therewasamaineffectofcultureinthepattern-matchingtask[F(1,69)54.29,p,.05]andaninteractionofagewithcul-tureinthedigitsymboltask[F(1,69)57.00,p,.05](seeHeddenetal.,2002).

StimuliInthisfMRIexperiment,fullcolorpicturesof200objectsand

200placesceneswereused(Figure1A;describedinmoredetailinGohetal.,2004)tocomposepicturestimuliofobjectsplacedwithincongruentbackgroundscenes.Pictureswerepresentedinquartets,whichresultedinfourexperimentalconditions:(1)fourrepeatedob-jectandscenepairs(OO:oldobject,oldscene);(2)repeatedobjectswithinfournovelscenes(ON:oldobject,newscene);(3)fournovelobjectswithinrepeatedscenes(NO:newobject,oldscene);and(4)fournovelobjectandscenepairs(NN:newobject,newscene).Theobjectssubtendedvisualanglesofapproximately0.5º31.0º(minimum)to2.5º35.5º(maximum)fromeachoftheircenters,whilebackgroundscenessubtendedavisualangleofapproximately4.6º36.3ºfromthefixationpoint.

Eachpicturewithinaquartetwaspresentedfor1.5secandsepa-ratedfromthenextpicturebyaninterpictureintervalof250msec(fixation;seeFigure1B).Quartetswerepseudorandomlypresentedsuchthatagivenconditiondidnotoccurmorethanthreetimescon-secutively.Quartetswerealsoseparatedbyinterquartetintervalsof

6,9,or12secwithameanseparationof9sec.ThejitteredintervalswerenecessaryforeffectiveestimationofBOLDresponsestothestimuliinthisrapid,event-relatedfMRIdesign(Dale,1999).

Functionalbrainimageswereacquiredaseachsubjectviewedthepicturestimulioveracourseoffourexperimentalrunsthatlasted348seceach.Eachruncomprised20quartets(5fromeachcon-dition),whichwereprecededandfollowedbyperiodsoffixationthatlasted30sectoallowforbetterestimationofbaselineBOLDresponses.Eachsubjectthereforeviewedatotalof20quartetsofeachexperimentalconditionacrossthefourruns.

Imaging ProtocolfMRIexperimentswereconductedattheCognitiveNeuroscience

LaboratoryinSingaporeandtheUniversityofIllinoisatUrbana-Champaign.Bothsitesusedidentical3.0TAllegrascanners(Sie-mens)andpersonnelworkedclosely together tobecertain thatprotocolsatthetwositeswereidentical.CriticalanalysesoffMRIsignal,noise,andstabilitywereperformed;theyshowedahighreli-abilityacrosssites(Suttonetal.,2007).1Fortheexperimentaltask,116functionalscanswereacquiredineachrunusingagradient-echoEPIsequencewithTRof3sec,FOV19.2319.2cm,anda64364matrix.Thirty-sixobliqueaxialslices,3mmthick(0.3mmgap)andapproximatelyparalleltotheAC–PCline,wereacquired.High-resolutioncoplanarT2anatomicaland3-DMPRAGEanatomicalimageswerealsoacquiredforimagecoregistrationofthefunctionalslicesinto3-Dspace.Stimuliwereprojectedontoascreenatthebackofthemagnetwhileparticipantsviewedthescreenusingamirror.

Image Data AnalysisFunctionalimageswereprocessedusingBrainVoyager20004.9

andBrainVoyagerQX1.3(BrainInnovation,Maastricht)custom-izedwithin-housescripts.GaussiansmoothinginthespatialdomainwasappliedusingaFWHMkernelof8mm.Functionaldatawerethenresampledinto13131mmresolutionpervoxel.Foreachofthefoursubjectgroups,thedatawereanalyzedusingagenerallinearmodel(GLM)comprisingsevenfiniteimpulseresponsepredictorsforeachofthefourexperimentalconditions(OO,ON,NO,andNN).ThuswemodeledtheevolutionoftheBOLDresponsetimecourseover21sec(sevenscans)fromstimulusonset.Subsequentcontrastanalysesofimagingdataconsideredonlythefourthpredictor(9secfromonset)foreachcondition,asthiswasidentifiedasthepeakresponsewithintheestimatedBOLDresponsetimecourseacrossallfourgroupsofsubjects(dataavailableuponrequest).Thisanalysis

resultedinastatisticalmapcontainingparameterestimatesforeachpredictorineveryvoxelofthe3-Dfunctionalbraindata.

Conjunction AnalysisAsinGohetal.(2004),weusedaconjunctionanalysisalongwith

aregionofinterest(ROI)approachtoidentifyandevaluateBOLDresponsesinobject,background,andbindingprocessingregions.Fortheconjunctionanalysis,wefirstcomputedvoxelmapscon-tainingtvaluesofeachcontrast(seebelow)ofparameterestimatesobtainedfromtheGLManalysis.Then,foreachvoxel,wecom-paredtherelevantcontrastsandenteredtheleastsignificanttvalueintoanewstatisticalvoxelmaponlyifallthecontrastsinconsid-erationwerepositive.Usingthisapproach,wedefined(1)object-processingvoxelsasthosethatshowedadaptationresponseswhenobjectswererepeatedregardlessofbackgroundrepetition(OO,NN;OO,NO;ON,NN;ON,NO);(2)background-processingvoxelsasthosethatshowedadaptationresponseswhenbackgroundswererepeatedregardlessofobjectrepetition(OO,NN;OO,ON;NO,NN;NO,ON);and(3)binding-processingvoxelsasthosethatshowedadaptationresponsesonlywhenbothobjectandbackgroundwererepeated,withtheadditionalrequirementthattheadaptationresponsesbegreaterthanthesumofpartialadaptationtoeitherobjectorbackgroundrepetitionalone(OO,NN;OO,ON;OO,NO;[OO,NN],[ON,NN]1[NO,NN]).Notethatbecausewewereconsideringadaptationresponses,thecontrastsaredescribedasattenuationsinsignal,ratherthanincreases(asismoretypical).

Next,theobject,background,andbindingROIsweredefinedascontiguousvoxels(thesmallestROIclusterconsistedof105voxels)thatshowedtherespectivesignificantconjunctionsatastatisticalthresholdofp,.001(uncorrected),exceptwhentheROIwasinthehippocampus,whereareducedthresholdofp,.005wasused(congruentwithproceduresusedbyothers:Eldridge,Knowlton,Furmanski,Bookheimer,&Engel,2000;Ojemannetal.,1997).TheseROIswereidentifiedseparatelyforthedatafromtheEastAsiangroupandthatfromtheWesterngroup.ExaminationofthepeakTalairachcoordinatesofthesefunctionalROIsinyoungandelderlyWesterners(seeTable2)showedthattheywerecomparablewiththoseoftheEastAsians(Cheeetal.,2006).2

Adaptation Magnitude AnalysisTocharacterizetheeffectsofageandcultureonthevisualpro-

cessingofobjects,backgroundscenes,andcontextualbinding,weevaluatedgroupdifferencesinadaptationmagnitudeineach

Table 1 Means (and Standard Deviations) for Demographic Information and Neuropsychological Test Scores

of Young and elderly Westerners and east Asian Subjects

Westerners EastAsians

Young Elderly Young Elderly(12males, (5males, (7males, (7males, FValues7females) 14females) 13females) 10females) Age3

M SD M SD M SD M SD Culture Age Culture

Age(years) 21.73 1.98† 68.10 5.53 21.30 1.11 66.65 4.00 – 2,709.5**0 –Yearsofeducation 15.26 1.38† 15.75 2.97 14.00 1.45 12.50 2.54 17.9** – –Patternmatching 36.13 7.39† 21.15 4.78 39.94 5.50 22.70 4.40 4.29* ,154.94** –Dotcomparison 16.07 1.87† 9.40 2.64 16.61 3.01 7.80 3.24 – ,138.98** –WAIS–RDigit–Symbol 72.93 9.36† 53.10 11.41 82.72 8.66 50.00 11.21 – ,116.46** 7.00**

WAIS–RInformation 22.93 3.47† 20.20 4.03 20.22 4.39 17.70 4.68 6.90* , 7.02** –WAIS–RComprehension 22.93 4.04† 21.05 3.53 21.28 3.72 23.05 4.88 – – –Mini-MentalStateExam 29.60 0.51† 29.00 1.12 29.39 0.92 28.30 1.38 – , 11.34** –WMS–IIIForwardSpatialSpan 10.14 2.19‡ 8.45 1.76 10.22 1.80 8.30 2.11 – , 11.76** –WMS–IIIBackwardSpatialSpan 9.71 1.49‡ 7.45 1.64 9.67 1.68 7.45 1.85 – , 23.15** –WAIS–IIIForwardDigitSpan 11.00 1.63‡ 10.00 2.85 12.39 2.38 10.50 1.85 – , 5.15** –WAIS–IIIBackwardDigitSpan 9.71 1.38‡ 6.70 2.49 9.22 2.44 6.40 1.90 – , 23.25** –

Note—OnlysignificantFvaluesarereportedforthemaineffectsofcultureandage,andtheinteractionbetweenageandculture.TestsarecompleteforallelderlysubjectsandallyoungEastAsiansanddataaremissingforsomeyoungWesterners. †n515. ‡n57. *p,.05. **p,.01.

48 goh et Al.

ofthefunctionalROIsasdefinedabove(seeEpstein,Higgins,&Thompson-Schill,2005,forasimilarapproach).WereasonedthatthedifferenceinBOLDresponseselicitedbytherelevantpairsofconditionsforeachfunctionalROIwouldgiveameasureofthein-tegrityoffunctionofthatregion,withlargeradaptationindicatingbetterfunctionalintegritythanweakorabsentadaptation.Intheobject-processingregions,adaptationmagnitudewasindexedbythedifferencebetweenONandNNresponses;inthebackground-processingregions,bythedifferencebetweenNOandNNresponses;andinthebindingregions,bythedifferencebetweenOOandNNresponses.NotethattheseROIwerealreadyidentifiedasbeinginvolvedinobject,background,andbindingprocessing,respec-tively.Thus,theresultingcontrastvalueswithineachROIreflect

thedegreeofattenuationinresponsetotherelevantrepeatedpicturecomponent(object,background,ortheassociationsbetweenthem)relativetowhennocomponentwasrepeated(NN).TheROImasksthatcharacterizedthelocusofeachfunctionalregionforEastAsiansandWesternerswereappliedtoeachoftherespectiveindividualsubjects.TheindividualmeasuresofmagnitudeofadaptationforeachROIweredeterminedandthedataobtainedweresubsequentlygroupedaccordingtoageandculture.

ReSulTS

We characterized the interaction between age andculturegroupusinganANOVAoftheadaptationmag-nitudedatafromallfourgroupsforeachROI(seeFig-ure2).Intheobject–backgroundbindingregions,weob-servedmaineffectsofageintherightparahippocampalgyrus[F(1,71)59.86,p,.001]andrighthippocampus[F(1,71)54.13,p,.05](Figure2A).Therewasnosig-nificantinteractionofagewithculture,suggestingthatreductionincontextualbindingisanage-relatedchangethatisindependentofculture.

Inthebackground-processingregions,therewerenosignificantdifferencesinadaptationresponseacrossallfourgroupsineithertherightorleftparahippocampalgyrus,suggestingthatbackgroundprocessingwaspre-servedacrossbothageandculture(Figure2B).

Ofparticularinterest,theanalysisofobject-processingregions showed evidence for a reduction of responsewith age in both left [F(1,71)5 11.24, p, .01] andright[F(1,71)510.85,p,.01]lateraloccipitalregions(Figure2C).There was also a marginally significantinteractionofagewithcultureintherightlateraloccipi-talregion[F(1,71)53.22,p,.08].Thisinteractionwaspredicted,andaplannedcomparisonofthiseffectinthisROIrevealedahighlysignificantdifferenceinobject-processingadaptationmagnitudesbetweenyoungandelderlyEastAsians[t(35)53.65,p,.001]butnotinyoungandelderlyWesterners[t(36)51.11,n.s.].More-over,theelderlyEastAsiansshowedsignificantlylowerobject-processingadaptationthandidelderlyWesterners[t(34)52.86,p,.05],whereastherewasnosignificantdifferencebetweenyoungEastAsiansandyoungWest-erners[t(37)50.01,n.s.].ThesamecomparisonsintheleftlateraloccipitalregionyieldedsignificantdifferencesasafunctionofageforbothWesterners[t(36)51.99,p,.05]andEastAsians[t(35)52.76,p,.01],withnoevidenceofaninteraction[F(1,71)50.07,n.s.].Overall,theanalysissuggeststhatobjectprocessinginthelateraloccipitalregionsisattenuatedinelderlyWesternersintheleftbutnottherightLOC,andgreatlyattenuatedinel-derlyEastAsiansinbothhemispheres.

DISCuSSION

Thepresentstudymakesthreemajorpointswithre-specttoneurocognitiveprocessesassociatedwithagingandculture;eachpointaddressesadifferentareaofven-tralvisualcortex.Thepatternofresultsobserveddemon-stratesthat(1)decreasesinneuralbindingprocessesaremanifestedcross-culturallyinelderlyadults;(2)neural

Table 2 Peak Talairach Coordinates of the Object, Background, and

Object–Background Binding ROIs Identified using the Conjunction Analysis for Young and elderly Westerners

BrainRegion

Brodmann’sArea

tValue

YoungSubjects

ObjectProcessing(NN.OOandNN.ONandNO.OOandNO.ON) Rinferioroccipitalgyrus 19 ]30 ]85 ]2 4.96 Linferioroccipitalgyrus 19 ]42 ]73 ]5 4.64 Rfusiformgyrus 37 ]45 ]67 ]2 4.52 Lfusiformgyrus 20 ]39 ]40 ]14 5.16

BackgroundSceneProcessing(NN.OOandNN.NOandON.OOandON.NO) Rparahippocampalgyrus 36 ]18 ]39 ]4 6.79 Lparahippocampalgyrus 36 ]22 ]43 ]5 5.73 Rlingualgyrus 19 ]13 ]68 ]6 4.52 Llingualgyrus 19 ]12 ]71 ]11 4.07 Rposteriorcingulate 29 ]10 ]48 ]8 5.34 Lposteriorcingulate 29 ]11 ]48 ]7 6.47 Lcuneus 18 ]6 ]92 ]9 4.21

ObjectandBackgroundSceneBinding(NN.OOandNO.OOandON.OOand[NN2OO].[NN2ON]1[NN2NO]) Rhippocampus 35 ]33 ]19 ]11 4.00 Rparahippocampalgyrus 37 ]29 ]49 ]11 6.86 Lparahippocampalgyrus 36 ]27 ]27 ]14 4.66 Rlingualgyrus 18 ]12 ]88 ]2 4.17 Lfusiformgyrus 37 ]30 ]70 ]11 3.97 Roccipito-parietalsulcus 19 ]49 ]73 ]12 3.11 Loccipito-parietalsulcus 19 ]36 ]79 ]19 4.61

ElderlySubjects

ObjectProcessing(NN.OOandNN.ONandNO.OOandNO.ON) Linferioroccipitalgyrus 19 ]45 ]74 ]5 4.17 Rfusiformgyrus 19 ]48 ]65 ]2 3.72 Lfusiformgyrus 37 ]39 ]43 ]17 3.85

BackgroundSceneProcessing(NN.OOandNN.NOandON.OOandON.NO) Rparahippocampalgyrus 36 ]24 ]44 ]8 4.15 Rlingualgyrus 19 ]20 ]70 ]11 4.17 Llingualgyrus 19 ]21 ]67 ]11 4.31 Rmiddleoccipitalgyrus 18 ]30 ]80 ]16 4.28 Lmiddleoccipitalgyrus 18 ]36 ]80 ]10 4.64

ObjectandBackgroundSceneBinding(NN.OOandNO.OOandON.OOand[NN2OO].[NN2ON]1[NN2NO]) RfusiformgyrusI 37 ]33 ]37 ]13 4.56 RfusiformgyrusII 19 ]30 ]67 ]8 3.48 Lfusiformgyrus 37 ]36 ]43 ]15 4.32 Roccipito-parietalsulcus 19 ]33 ]73 ]22 3.45 Loccipito-parietalsulcus 19 ]33 ]70 ]28 3.44

processingofbackgroundscenesincomplexpicturesisunaffectedbyageorculture;and(3)object-processingre-gionsdeclinewithage,disproportionatelyinEastAsians.Eachresultisdiscussedinturn.

Binding Mechanisms Across Age and Cultural Group

Thefindingthat,duringpassiveviewingofpictures,bothelderlyEastAsiansandelderlyWesternersshoweddecreasedbindingintherighthippocampusandrightpara-hippocampalgyruscomparedwithyoungadultssuggeststhatexperience(intheformofculturalexposure,forex-ample)mayplayonlyarelativelymodestroleinmoderat-ingthebindingprocessandthatbiologicalmechanismsassociatedwiththeagingprocessmayplayalargerroleindecreasingolderadults’abilitytoengagemedialtemporalstructuresforbindingtothesamedegreethatyoungadults

do.Studieshaveshownthatthehippocampusandentorhi-nalcortexundergoatrophywithageandthatthisatrophycanberelatedtopoorermemoryperformance(Rodrigue&Raz,2004;Rosenetal.,2003).Thelossofneuraltissueavailableforprocessingcontextualbindingmaydiminishthequalityoftherepresentationsofassociativeinforma-tionthatareencodedandsubsequentlyaccessed.Thefind-ingofthisreducedbindinginolderadultsreplicatesthere-sultsofMitchell,Johnson,Raye,Mather,andD’Esposito(2000),inwhichanintentionalencodingtaskwasused.TheresultsofthepresentstudyandthoseinCheeetal.(2006)extendthisfindingtoapassiveviewingtask.

Age, Cultural Group, and the Processing of Background Context

Wefoundlittleevidencethatneuralareasthatarespe-cializedforbackgroundsceneprocessingdifferasafunc-

AR Hippocampus0.50

R Parahippocampal Gyrus1.50

Object–BackgroundBinding

BL Parahippocampal Gyrus1.00

R Parahippocampal Gyrus1.00

Background SceneProcessing

z = –4

x = 30

CL Lateral Occipital Region1.00

R Lateral Occipital Region1.00

Object Processing

z = –7

Young Americans Elderly Americans Young East Asians Elderly East Asians

Figure 2. Mean magnitude of adaptation in young east Asians, young Westerners, elderly east Asians, and elderly Westerners. (A) Responses in hippocampal (left panel) and parahippocampal (right panel) binding regions. (B) Re-sponses in left and right parahippocampal areas engaged in background processing. (C) Responses in left and right lateral occipital complex engaged in object processing. Standard error bars are shown.

50 goh et Al.

tionofageorculture,althoughsomefurtherexplorationresultedinsomemarginallysignificanteffectsintheex-pecteddirection.WenotedthatthebackgroundadaptationresponseintheleftparahippocampalgyruswasslightlylowerforelderlyWesternersthanforyoungWesterners[t(36)51.62,p5.06]andyoungEastAsians[t(37)51.37,p5.09],whereastherewasnosignificantcontrastbetweenelderlyEastAsianscomparedwithyoungWest-erners[t(34)51.02,n.s.]andyoungEastAsians[t(35)50.72,n.s.].ThisfindingisconsistentwiththenotionofpreservedbackgroundprocessinginelderlyEastAsians.That the relatively equivalent background processingacrossgroupsinthisstudymayresultfromeffectivepro-cessingofcontextualinformationincomplexscenesbyolderadults.

Thereisconsiderableevidencethatolderadultsbut-tresstheirmemoryforcomplexpicturesbyusingcon-textualinformationwhenitispresentinpicturesthataresufficientlyrichinmeaninganddetail(Park,Puglisi,&Smith,1986;Park,Smith,Morrell,Puglisi,&Dudley,1990;Smith,Park,Cherry,&Berkovsky,1990). It ispossiblethatfurtherexplorationofneuralprocessingofcontextwilldemonstrateagedifferencesinthismecha-nismincasesinwhichthecontextualinformationislessmeaningfulormorepoorlyintegratedwiththetarget.Inparticular,alargenumberoffindingssuggeststhatolderadultsremembercontextualinformationassociatedwithwordsorabstractpictureslesswellthanyoungadultsdo(Parketal.,1990;Smithetal.,1990).Itmayalsobethatpronouncedculturaldifferencesintheneuralprocessingofbackgroundinformationwillsimilarlyemergeundermoredemandingconditions,accentuatingtheexpectedbiasforEastAsianculturalgroupstoshowapreferen-tialprocessingofbackgrounddetailrelativetoWesterngroups.

Age, Culture, and Object ProcessingInthepresentstudy,wefoundevidencefordiminished

objectprocessingintheLOCinolderadultsfrombothcultures,asreportedinitiallybyCheeetal.(2006).Per-hapsthemostimportantfindingfromthepresentstudyisthatelderlyWesternersshowedsignificantlygreaterobject-processingadaptationintheLOCthandidelderlyEastAsians,whoshowedalmostnoadaptationwhatso-ever.ThisfindingprovidesneuroimagingevidenceforculturalbiasesinperceptualprocessingofobjectsandisinagreementwithGutchessetal.(2006),whoreportedgreaterneuralengagementforobject-processingregionsinWesternersthaninEastAsiansinapicturerecognitiontask,albeitforyoungadultsinbothcases.AlthoughthestimuliusedinthisstudyweresimilartothoseusedbyGutchessetal.,thepresentstudydifferedinthatweusedapassiveviewingtaskandanadaptationparadigmasop-posedtoadirectedincidentalencodingtask.

Perhapsbecausethepresentparadigmiscomparativelysubtle,culturaldifferencesbecameapparentonlyinoldersubjectswhohadhadmoreexposuretotheirrespectivecul-turalenvironmentsthantheyoungsubjectshadhad.Thisisaplausibleexplanation,sincethereissubstantialevidencethatneuro-anatomicalchangesinthebrainarerelatedto

thelengthoftimeindividualsspendbeingengagedinspe-cificbehavioralpracticesandsensoryenvironments.InastructuralMRIstudy,posteriorhippocampalvolumewaspositivelycorrelatedwithspatialnavigationexperienceinLondontaxicabdriversversuscontrols(Maguireetal.,2003).Recently,Schneideretal.(2005)alsoshowedthatthevolumeofHeschl’sgyruswaspositivelycorrelatedwithmusicalexperienceinprofessionalmusiciansversusnonmusicians.Likewise,compellingevidenceforfunc-tionalchangesinrelationtoexperienceisclearlyseeninthefunctionalspecializationofbrainregionsforletterandnumberrecognitioninhumansubjects(Polk&Farah,1995;Polketal.,2002;Puce,Allison,Asgari,Gore,&McCarthy,1996).Wepositthatculturallydistinctbehav-iorsandthoughtcanalsobeconstruedasdifferencesinspecificexperiencesthataffectneuralfunction.Analter-nateexplanationtotheculturalexperiencehypothesisisthatAsiansocietyischangingrapidlyandthattheyoungSingaporeans(allofChinesedescent)haveinternalizedWesternvaluestothepointthattheynolongerdisplaybehavioralpatternscharacteristicofAsiancultures.Evenifthisisthecase,theresultsclearlydemonstratesystem-aticdifferencesbetweenEasternandWesternsubjects,withabiastowardmoreprocessingofobjectinforma-tioninelderlyWesterners,afindinginagreementwiththecultural/cognitiveframeworkproposedbyNisbettandMasuda(2003).

ConclusionInsummary,thepresentfindingssuggestthatagealone

cannotexplainthereducedexpressionofobject-processingregionsinelderlyEastAsiansandthatthefunctionalen-gagementofneuralareas,suchastheLOC,canbemodi-fiedthroughexperience.Themostplausiblebasisforthedifference,basedontheburgeoningliteratureinculturalpsychology,appearstobethatvisualexperienceisbiasedbycultural factors.Futureresearch isneeded tomorespecificallydeterminedifferencesinneuralcircuitrythatvaryasafunctionofexperience,withculturaldifferencesplayingaplausibleroleinshapingprocessesthatarebothperceptual,asinthepresentstudyofobjectandscenepro-cessingduringpassiveviewing,aswellasstrategic,asreportedbyGutchessetal.(2006).

AuTHOR NOTe

ThisworkwassupportedbyBMRCGrant04/1/36/19/372toM.W.C.aswellasbyNationalInstituteonAgingGrantsR01AGO15047andR01AGO60625-15toD.C.P. E.D.L.wassupportedbyNationalInstituteofMentalHealthTrainingGrantT32MH19554.Correspondenceconcern-ingthisarticleshouldbeaddressedtoD.C.Park,BeckmanInstitute,405NorthMathews,Urbana,IL61801(e-mail:denisep@uiuc.edu).

ReFeReNCeS

Chalfonte, B. L., & Johnson, M. K. (1996).Featurememoryandbind-inginyoungandolderadults. Memory & Cognition, 24,403-416.

Chee, M. W., Goh, J. O., Venkatraman, V., Tan, J. C., Gutchess, A., Sutton, B., et al. (2006).AgerelatedchangesinobjectprocessingandcontextualbindingrevealedusingfMR-adaptation. Journal of Cognitive Neuroscience, 18,495-507.

Chiu, L. H. (1972).Across-culturalcomparisonofcognitivestylesinChineseandAmericanchildren. International Journal of Psychology, 7,235-242.

Chua, H. F., Boland, J. E., & Nisbett, R. E. (2005).Culturalvaria-tionineyemovementsduringsceneperception. Proceedings of the National Academy of Sciences, 102,12629-12633.

Crum, R. M., Anthony, J. C., Bassett, S. S., & Folstein, M. F. (1993).Population-basednormsfortheMini-MentalStateExamina-tionbyageandeducationallevel. Journal of the American Medical Association, 269,2386-2391.

Dale, A. M. (1999).Optimalexperimentaldesignforevent-relatedfMRI. Human Brain Mapping, 8,109-114.

Eldridge, L. L., Knowlton, B. J., Furmanski, C. S., Bookheimer, S. Y., & Engel, S. A. (2000).Rememberingepisodes:Aselectiveroleforthehippocampusduringretrieval. Nature Neuroscience, 3,1149-1152.

Epstein, R. [A.], Graham, K. S., & Downing, P. E. (2003).Viewpoint-specificscenerepresentations inhumanparahippocampalcortex. Neuron, 37,865-876.

Epstein, R. A., Higgins, J. S., & Thompson-Schill, S. L. (2005).Learningplacesfromviews:Variationinsceneprocessingasafunc-tionofexperienceandnavigationalability. Journal of Cognitive Neuro-science, 17,73-83.

Epstein, R. [A.], & Kanwisher, N. (1998).Acorticalrepresentationofthelocalvisualenvironment. Nature, 392,598-601.

Goh, J. O., Siong, S. C., Park, D., Gutchess, A., Hebrank, A., & Chee, M. W. (2004).Corticalareasinvolvedinobject,background,andobject-backgroundprocessingrevealedwithfunctionalmagneticresonanceadaptation. Journal of Neuroscience, 24,10223-10228.

Gong, Y. (1983).RevisionofWechsler’sAdultIntelligenceScaleinChina.Acta Psychologica Sinica, 15,362-370.

Grill-Spector, K., Kourtzi, Z., & Kanwisher, N. (2001).Thelateraloccipitalcomplexanditsroleinobjectrecognition. Vision Research, 41,1409-1422.

Grill-Spector, K., & Malach, R. (2001).fMR-adaptation:Atoolforstudyingthefunctionalpropertiesofhumancorticalneurons. Acta Psychologica, 107,293-321.

Gutchess, A. H., Welsh, R. C., Boduroglu, A., & Park, D. C. (2006).Culturaldifferencesinneuralfunctionassociatedwithobjectprocess-ing. Cognitive, Affective, & Behavioral Neuroscience, 6, 102-109.

Hedden, T., Park, D. C., Nisbett, R. [E.], Ji, L.-J., Jing, Q., & Jiao, S. (2002).Culturalvariationinverbalversusspatialneuropsychologicalfunctionacrossthelifespan. Neuropsychology, 16,65-73.

Henke, K., Weber, B., Kneifel, S., Wieser, H. G., & Buck, A. (1999).Humanhippocampusassociatesinformationinmemory. Proceedings of the National Academy of Sciences, 96,5884-5889.

Ji, L.-J., Zhang, Z., & Nisbett, R. E. (2004).Isitcultureorisitlan-guage?Examinationoflanguageeffectsincross-culturalresearchoncategorization. Journal of Personality & Social Psychology, 87,57-65.

Joseph, J. E., & Gathers, A. D. (2003).Effectsofstructuralsimilarityonneuralsubstratesforobjectrecognition.Cognitive, Affective, & Behavioral Neuroscience, 3,1-16.

Madden, D. J., & Langley, L. K. (2003).Age-relatedchangesinselec-tiveattentionandperceptualloadduringvisualsearch. Psychology & Aging, 18,54-67.

Maguire, E. A., Spiers, H. J., Good, C. D., Hartley, T., Frackowiak, R. S., & Burgess, N. (2003).Navigationexpertiseandthehumanhippocampus:Astructuralbrainimaginganalysis. Hippocampus, 13,250-259.

Malach, R., Reppas, J. B., Benson, R. R., Kwong, K. K., Jiang, H., Kennedy, W. A., et al. (1995).Object-relatedactivityrevealedbyfunctionalmagneticresonanceimaginginhumanoccipitalcortex. Proceedings of the National Academy of Sciences, 92,8135-8139.

Masuda, T., & Nisbett, R. E. (2001).Attendingholisticallyversusana-lytically:ComparingthecontextsensitivityofJapaneseandAmeri-cans. Journal of Personality & Social Psychology, 81,922-934.

Maylor, E. A., & Lavie, N. (1998).Theinfluenceofperceptualloadonagedifferencesinselectiveattention. Psychology & Aging, 13,563-573.

McCarley, J. S., Mounts, J. R., & Kramer, A. F. (2004).Age-relateddifferencesinlocalizedattentionalinterference. Psychology & Aging, 19,203-210.

McGonigle, D. J., Howseman, A. M., Athwal, B. S., Friston, K. J., Frackowiak, R. S., & Holmes, A. P. (2000).VariabilityinfMRI:Anexaminationofintersessiondifferences.NeuroImage, 11,708-734.

Milham, M. P., Erickson, K. I., Banich, M. T., Kramer, A. F., Webb, A., Wszalek, T., & Cohen, N. J. (2002).Attentionalcontrolintheagingbrain:InsightsfromanfMRIstudyoftheStrooptask. Brain & Cogni-tion, 49,277-296.

Mitchell, K. J., Johnson, M. K., Raye, C. L., & D’Esposito, M. (2000).fMRIevidenceofage-relatedhippocampaldysfunctioninfeaturebindinginworkingmemory. Cognitive Brain Research, 10,197-206.

Mitchell, K. J., Johnson, M. K., Raye, C. L., Mather, M., & D’Esposito, M. (2000).Agingandreflectiveprocessesofworkingmemory:Bindingandtestloaddeficits. Psychology & Aging, 15,527-541.

Naveh-Benjamin, M., Hussain, Z., Guez, J., & Bar-On, M. (2003).Adultagedifferencesinepisodicmemory:Furthersupportforanassociative-deficithypothesis. Journal of Experimental Psychology: Learning, Memory, & Cognition, 29,826-837.

Nisbett, R. E., & Masuda, T. (2003).Cultureandpointofview. Pro-ceedings of the National Academy of Sciences, 100,11163-11170.

Nisbett, R. E., & Miyamoto, Y. (2005).Theinfluenceofculture:Ho-listicversusanalyticperception. Trends in Cognitive Sciences, 9,467-473.

Nisbett, R. E., Peng, K., Choi, I., & Norenzayan, A. (2001).Cultureandsystemsofthought:Holisticversusanalyticcognition. Psycho-logical Review, 108,291-310.

Ojemann, J. G., Akbudak, E., Snyder, A. Z., McKinstry, R. C., Raichle, M. E., & Conturo, T. E. (1997).Anatomiclocalizationandquantitativeanalysisofgradientrefocusedecho-planarfMRIsus-ceptibilityartifacts. NeuroImage, 6,156-167.

Park, D. C., Puglisi, J. T., & Smith, A. D. (1986).Memoryforpictures:Doesanage-relateddeclineexist? Psychology & Aging, 1,11-17.

Park, D. C., Puglisi, J. T., & Sovacool, M. (1984).Picturememoryinolderadults:Effectsofcontextualdetailatencodingandretrieval. Journal of Gerontology, 39,213-215.

Park, D. C., Smith, A. D., Morrell, R. W., Puglisi, J. T., & Dudley, W. N. (1990).Effectsofcontextualintegrationonrecallofpicturesinolderadults.Journal of Gerontology, 45,P52-P58.

Polk, T. A., & Farah, M. J. (1995).Lateexperiencealtersvision. Na-ture, 376,648-649.

Polk, T. A., Stallcup, M., Aguirre, G. K., Alsop, D. C., D’Esposito, M., Detre, J. A., & Farah, M. J. (2002).Neuralspecializationforletterrecognition. Journal of Cognitive Neuroscience, 14,145-159.

Pringle, H. L., Irwin, D. E., Kramer, A. F., & Atchley, P. (2001).Theroleofattentionalbreadthinperceptualchangedetection. Psycho-nomic Bulletin & Review, 8,89-95.

Puce, A., Allison, T., Asgari, M., Gore, J. C., & McCarthy, G. (1996).Differentialsensitivityofhumanvisualcortextofaces,letter-strings,andtextures:Afunctionalmagneticresonanceimagingstudy. Journal of Neuroscience, 16,5205-5215.

Rodrigue, K. M., & Raz, N. (2004).Shrinkageoftheentorhinalcortexoverfiveyearspredictsmemoryperformanceinhealthyadults. Jour-nal of Neuroscience, 24,956-963.

Rosen, A. C., Prull, M. W., Gabrieli, J. D. E., Stoub, T., O’Hara, R., Friedman, L., et al. (2003).Differentialassociationsbetweenento-rhinalandhippocampalvolumesandmemoryperformanceinolderadults. Behavioral Neuroscience, 117,1150-1160.

Salthouse, T. A. (1996).Theprocessing-speedtheoryofadultagedif-ferencesincognition. Psychological Review, 103,403-428.

Schneider, P., Sluming, V., Roberts, N., Scherg, M., Goebel, R., Specht, H. J., et al. (2005).StructuralandfunctionalasymmetryoflateralHeschl’sgyrusreflectspitchperceptionpreference. Nature Neuroscience, 8,1241-1247.

Smith, A. D., Park, D. C., Cherry, K., Berkovsky, K. (1990).Agedifferencesinmemoryforconcreteandabstractpictures.Journal of Gerontology, 45,P205-P209.

Spencer, W. D., & Raz, N. (1995).Differentialeffectsofagingonmemoryforcontentandcontext:Ameta-analysis. Psychology & Aging, 10,527-539.

Sutton, B. P., Goh, J., Hebrank, A., Colcombe, S., Welsh, R., Chee, M., & Park, D. C. (2007).Investigation and validation of in-tersite fMRI studies using same imaging hardware.Manuscriptinpreparation.

Wechsler, D. (1981).WAIS–R manual:Wechsler Adult Intelligence Scale–Revised. SanAntonio,TX:PsychologicalCorporation.

52 goh et Al.

1.Magnetcomparabilitywasassessedbyhumanandphantomexperi-ments.ComparabilityoftheBOLDresponseswasaddressedbyscan-ningtwosubjects(whowerenotpartofthemainstudy)repeatedlyatbothsitesonamotorandvisualtask(McGonigleetal.,2000).Fifteenrunsofeachtaskateachsitewereperformed.Voxel-by-voxelwholebrainANOVAandICCanalysesusingtask,subject,andscannersitesasfactorswereperformedonthedata;theseanalysesindicatedhighreli-abilityacrosssites.Specifically,taskandsubjectaccountedforamuchgreaterproportionofthevarianceinthedatathandidsite.

2.TheROIwereidentifiedseparatelyacrossgroups,sinceacom-plete,whole-groupGLMrequiredadatasetthatrequiredalargeamount

ofcomputermemory,whichthecurrentsoftwaredoesnotallow.WeidentifiedtheROIbyanalyzingtheEastAsiansandWesternersassepa-rategroups.Wealsoperformedtheanalysisbyconsideringfourgroupsacrossageandculture.Althoughtherewereslightdifferencesinpeakvoxellocations,theresultswerelargelysimilaracrossgroups.Wereporthereonlytheformeranalysis,sinceitallowsustoidentifyandexaminetheBOLDresponsesintheobject-processingROIintheelderlyEastAsians,whichisabsentwhenanalyzingthatdatasetalone.

(ManuscriptsubmittedMarch16,2006;revisionacceptedforpublicationAugust1,2006.)

Age and culture modulate object processing and … · on physical features and categorical...

Documents