The effect of word concreteness on recognition memory - PDF document

TheeffectofwordconcretenessonrecognitionmemoryK.Fliessbach,S.Weis,P.Klaver,C.E.Elger,andB.WeberUniversityofBonn,DepartmentofEpileptology,Sigmund-Freud-Str.25,D-53105Bonn,GermanyLifeandBrainCenter,DepartmentofNeuroCognition,Sigmund-Freud-Str.25,D-53105Bonn,Germany www.elsevier.com/locate/ynimgNeuroImage32(2006)1413 Correspondingauthor.DepartmentofEpileptology,UniversityofBonn,SigmundFreud-Str.25D-53105Bonn,Germany.Fax:+492286885264.E-mailaddress:klaus.fliessbach@ukb.uni-bonn.de(K.Fliessbach).AvailableonlineonScienceDirect(www.sciencedirect.com). derivative.ForfMRIanalysis,correctanswersweredefinedaspreviouslystated(i.e.confidentlygivenoldjudgementsforoldwords=hits;confidentlygivennewjudgementsfornewwords=correctrejections),whereasformistakesunconfidentlygivenwronganswerswerealsocounted(i.e.alloldjudgementsfornewwords=falsealarms;allnewjudgementsforoldwords=misses).Thiswasnecessarybecauseotherwisethenumberofeventsineachcategorywouldhavebeentoosmallinmanysubjects.Correctresponseswhichwerenotgivenconfidentlyweremodelledseparatelyandwerenotincludedinthestatisticalanalysis.Formodellingtheencodingperiod,sixvectorsofstimulusonsetswereused(abstract/concretewordsthatwereeitherhits,missesorcorrectresponsesnotgivenconfidently).Whenmodel-lingtherecognitionperiod,tendifferentvectorswereconstructed(abstract/concretewordsthatwerehits,misses,correctrejections,falsealarmsorcorrectresponsesnotgivenconfidently).Parameterimagesfortherespectivecontrastsofinterestweregeneratedforeachsubjectandwerethensubjectedtoasecond-levelrandomeffectsanalysisusingaone-wayanalysisofvariance(within-subjectANOVA)asamodel.Thepredefinedlinearcombinationsofthegroupcontrastimageswerethentestedwithaonesampletestagainstanullhypothesisofnoeffect.Themaincontrastsweredefinedasfollows(inbracketsgiventheexperimentalpart):WordtypeeffectsConcretenesseffect:concrete�abstractwordsAbstractnesseffect:abstract�concretewordsMemoryeffectsSubsequentmemoryeffect(learning):hits�missesNegativesubsequentmemoryeffect(learning):misses�hitsOld/New-effect(recognition):hits�correctrejectionsNew/Old-effect(recognition)correctrejections�hits Table1Memoryperformanceandreactiontimes(RT)forconcreteandabstractwordsConcreteAbstractPercentageRT(ms)PercentageRT(ms)StudiedwordsHits59.7±19.41307±56555.6±18.91363±544Misses13.3±12.11582±71511.4±13.21498±750responses13.7±8.52018±74217.1±8.52048±786responses12.1±7.61889±74514.9±9.81818±706WordsnewattestCorrectrejections43.6±17.41577±65340.4±19.21627±682Falsealarms9.1±7.51497±59113.4±9.01491±542responses30.9±13.31830±76429.0±15.21826±736responses14.0±7.11967±70815.7±8.02029±770 Fig.1.Statisticalparametrict-mapforabstract�concretewords(a)andhits�misses(subsequentmemoryeffect)(b)duringencoding(threshold0.001),projectedontoa3D-reconstructionofacanonicalsinglesubjectbrain.K.Fliessbachetal./NeuroImage32(2006)1413 Positivememoryeffect(recognition):hits�missesNegativememoryeffect(recognition):misses�hitsInteractionsbetweenthewordtypeeffectsandthedifferentmemoryeffectswerecalculatedaccordingly.Thestatisticalthresholdwassetata-valueof0.001voxelwise(uncorrected)withaclusterextentof�9contiguousvoxelsandonlyclustersat0.05attheclusterlevel(correctedformultiplecomparisons)wereconsideredsignificant.Totestforregionaloverlapsbetweenwordtypeandmemoryeffects,wordtypeeffects(threshold0.001)wereinclusivelymaskedwiththememoryeffectswitha-value0.05.Tomorespecificallytestfordifferencesinmemoryeffectsforthetwowordtypestheseparateold/new-effectforabstractandconcretenounsduringtherecognitionperiod0.001)wereinclusivelymaskedwithwordtypeeffectsfromtheencodingperiod(maskthreshold0.05).Totestforbrainareasassociatedwithinter-individualdifferencesinthememoryconcretenesseffect,asecond-levelcorrelationanalysiswasperformed.Thet-mapsforthesubsequentmemoryeffectduringlearningandtheoldneweffectduringrecognitionwerecorrelatedwiththeextentoftheconcretenesseffectoversubjects.Theextentoftheconcretenesseffectwasdefinedasthecorrectedrecognitionrateforconcretewordsminuscorrectedrecognitionrateforabstractwords.Forthisanalysis,activationsofatleasttenadjacentvoxelsatasignificancelevelof0.001withoutanyfurthercorrectionwereinterpreted.AnatomicalclusterlabellingwasdoneusingtheAnatomicalAutomatedLabelingToolforSPM(Tzourio-Mazoyeretal.,2002ForthetransformationofMNI-coordinatesinTailerach(TAL)-Coordinatesweusednon-lineartransformationaccordingto:www.cbu.cam.ac.uk/imaging/common/mnispace.shtmlMemoryperformanceThecorrectedrecognitionrate(hitsfalsealarms)wassig-nificantlyhigherforconcretewordsthanforabstractwords(50.6±21.9%vs.42.1±22.2%,=3.0,=0.007).Thisdifferencewasmainlybasedonasignificantlysmallerrateoffalsealarmsforconcretewordsthanforabstractwords(9.1±7.5%vs.13.4±9.0%,2.7,=0.015),whereastherateofhitsdidnotdiffersignificantly(59.7±19.4vs.55.6±18.9,=1.6,n.s.).Thepercen-tageofcorrectrejectionsandmissesdidnotdiffersignificantlyeither.Thereactiontimesfortheold/new-judgementweresignificantlyshorterforconcretewordsthanforabstractwords(1600±714msvs.1642±713ms,=2.5,=0.013).DetailedresultsareshowninTable1Thecontrastabstractvs.concretewordsyieldedasignificantactivationoftheleftinferiorfrontalgyrus(BrodmannArea(BA)45)(Fig.1Table2).Therewerenoareasdisplayingsignificantactivationfortheoppositecontrast.Thecomparisonofsubsequentlyremembered(hits)versusforgottenwords(misses)(subsequentmemoryeffect)showedfourclustersofactivationbilaterallyintheinferiorandmiddlefrontalgyri(Table2).Therewasnosignificantactivationfortheoppositecontrast(negativesubsequentmemorycontrast).Theareaactivatedbytheabstractvs.concretecontrastwasoverlappingwiththeleftinferiorfrontalareaseenwiththesubsequentmemorycontrastsothatafterinclusivelymaskingthefirstcontrastwiththelatter,thisareastillshowedsignificantactivation(Fig.2).Leftinferiorfrontalactivationwasalsofoundwhenthesubsequentmemorycontrastforabstractwordsalonewasmaskedwiththecontrastabstractvs.concretewords,althoughthiscomparisonwasnotsignificantataclusterlevel.Therewerenosignificantinteractionsbetweenwordtypeandmemoryeffects.Duringrecognition,theactivationpatternfortheabstractvs.concretewordswassimilartothatduringencodingwithasignificantactivationofthetriangularpartoftheleftinferiorfrontalgyrus(BA45)(notshown).Theconcretevs.abstractcontrastshowedabilateralposterioractivationinvolvingtheangulargyrusonbothsides,togetherwithpartsoftheinferiorparietallobeontheleftside.Besideshand-motoractivityforthebuttonpressesononeside,theold/new-effectyieldeda Table2ActivationclustersformaineffectsBrainregionTAL-coordinatesnzPxyzAbstract�concreteL.inferiorfrontalg.(BA45)502171314.250.016Concrete�abstractNosignificantactivationSubsequentmemoryeffectR.inferiorfrontalg.(BA45)5024241524.90.009L.inferiorfrontalg.(BA44)486301554.460.008R.inferiorfrontalg.(BA44)452341094.270.031L.inferiorfrontalg.(BA45)501781883.950.003Abstract�concreteL.inferiorfrontalg.(BA45)482472154.40.003Concrete�abstractL.parietalinf.G.77402564.250.001L.angularg.65393.78R.angularg.4569391184.100.031Old/new-effectR.precentralg.4212483484Inf0.001L.precuneus365345.7L.cerebellarhemisphere51224166.40.001R.rolandicoperculum4214154485.890.001L.angularg.65426305.860.001L.supramarginalg.45333.58R.anteriorcingulateg.63844914.780.001L.anteriorcingulateg.03894.59R.caudaten.61161654.710.009L.inferiorfrontalg.(BA45)383841604.450.010R.thalamus1541223.970.028BrainregionsandTAL-coordinatesofactivationmaxima.Notethatonlyclustersthatweresignificantonaclusterlevelof0.05(correctedformultiplecomparisons)arelisted.Localmaximaofsubclustersarelistedwhentheyaremorethan8mmapartfromthemainpeakactivation.=numberofsuprathresholdvoxels,-scoreatpeakactivation,-valueforthecluster(correctedformultiplecomparisons).K.Fliessbachetal./NeuroImage32(2006)1413 semanticprocessingthanconcretewordsasapremiseforsuccessfulencoding.Onepossibleexplanationforthiscouldbeasupportiveroleofotherbrainareasfortheencodingofconcretewords.However,ourencodingdataoffernopositiveevidenceforthisassumptionsincetherewerenoadditionalbrainareasactivatedmorestronglybyconcretewords.Duringrecognitionweobservedstrongerbilateralactivationoftheinferiorparietalcortexandtheangulargyrusforconcretevs.abstractwords.Thisfindingisinlinewitharecentstudyonconcretewordprocessingwithoutmemoryretrieval(Binderetal.,).Ourstudydesignallowedustoshowthattheleftparietalactivationwasalsoassociatedwithsuccessfulrecognitionirrespectiveofwordtype.Thisfindingisnotunexpectedsincethisregionisoftenfoundtobeassociatedwithcorrectrecognitioninrecognitionmemoryparadigms(e.g.Weisetal.,2004;Hensonetal.,2005).Moreprecisely,theregionfoundinourstudyroughlycorrespondstoaregionproposedtobespecificfortherecollectionofamemoryasopposedtomerefamiliarity(WheelerandBuckner,).Theinterpretabilityofthisactivationislimitedbythefactthatitcouldhavereflecteddifferencesinmemorylevelforconcreteandforabstractwords.However,thisactivationisalsopresentforcorrectlyrejectedconcretevs.abstractwordsduringrecognition.Thus,thisactivationseemstobedrivennotonlybythecorrectidentificationofstudiedwords,butalsobytheprocessingofconcretewordsperseunderarecognitiontask.Thiscouldmeanthatconcretewordsmightbebettersuitedtoevokespecificcontextualinformation,whichissupposedtobethebasisofrecollection.Moredirectevidenceforbrainregionsbeingdifferentiallyinvolvedinencodingandretrievalofconcreteandabstractwordswasfoundbyanothermaskingprocedureusingthewordtypeeffectsfromtheencodingperiodasamaskforthewordtypespecificold/new-effectsduringretrieval.Forconcretewords,thisanalysisyieldedsignificantactivationsintheleftandrightanteriorprecuneus,theleftcerebellarhemisphere,andbilateralposteriorandanteriorcingulatecortex.ThefindingofaprecuneusactivationisinlinewithfindingsfromclassicPET(Fletcheretal.,1996)andfMRIstudies(Hensonetal.,1999)thatsuggestedarolefortheprecuneusintheretrievalofimageablematerial.Meanwhile,studieshavesuggestedafunctionaldissociationwithintheprecuneus,withamoreposteriorregionbeinginvolvedinretrievingmoreabstractcontents,andamoreanteriorregionbeinginvolvedintheretrievalofmorevisualcontents(Lundstrometal.,2003,Woodruffetal.,2005).Thebilateralregionfoundtobemorestronglyinvolvedinsuccessfulretrievalofconcretevs.abstractwordsinourstudycorrespondstothelatter.Strongeractivationsinthisregionwerealsopresentduringtheintentionalencodingofconcreteascomparedtoabstractwords,whichisinlinewithpreviousstudiesonconcretewordprocessing(Binderetal.,2005Thisfindingsupportstheideaofa(contentspecific)reinstatementofneuronalactivityfromtheencodingperiodwhilesuccessfullyretrievingthisinformation.Itfurthermoresupportsthenotionofanadditional,imagery-basedsystemfortheencodingofconcretewords,asproposedbydual-codingtheory,althoughtheroleoftheprecuneusinthiscontextmustbefurtherclarified(forarecentreview,seeCavannaandTrimble,2006).Itmustalsobestressedthatourresultsdonotshowthatthespecificreinstatedbrainactivitiesareforsuccessfulrecollectiontheycouldalsobeinterpretedasaconsequenceofretrievalsuccess(foramoredetaileddiscussionofthisaspectseeWoodruffetal.,2005Activationsofthecerebellarhemispheresduringepisodicmemoryretrievalhavebeendescribedbeforeinanumberofstudies(e.g.Weisetal.,2004,Cabezaetal.,2002).However,theexactroleofthecerebelluminrecognitionmemoryispoorlyunderstood.Sincecerebellarlesionsdonothaveamajorimpactonmemoryperformance,aratherunspecificsupportingroleiswidelyassumed.Withrespecttoconcretewordprocessing,cerebellaractivityhasnotbeenreported,whichcouldbepartlyduetothefactthatthecerebellumisrarelyfullycoveredinimagingstudies.BecausethecerebellumisknowntobeinvolvedinmotorimageryRossetal.,2003),wespeculatethatthisactivationisduetotheinductionofimaginedmanipulationsbyconcretewordssuchastools.Thisquestioncouldbefurtheraddressedbyamorespecificitemselectionthatallowsadistinctionbetweendifferentclassesofconcretewords.Posteriorandanteriorcingulateactivationshavealsobeenlinkedtoretrievalsuccessinpreviousstudies.Posteriorcingulateactivationsareregularlyfoundincombinationwithprecunealand Fig.5.Left:statisticalparametrict-mapforthecorrelationbetweenestimatesoftheold/neweffectandthebehavioralconcretenesseffect(0.001),projectedontoacanonicalsinglesubjectT1-weightedimage.Right:scatterplotofthecontrastestimatesagainsttheconcretenesseffect(correctedrecognitionrateforconcretewordsminuscorrectedrecognitionrateforabstractwords)attheactivationmaximum(TAL-coordinatesK.Fliessbachetal./NeuroImage32(2006)1413 leftlateralparietalactivations(Wagneretal.,2005)andmightreflectsimilarprocessesasdiscussedpreviously.Anteriorcingulateactivationsinarecognitionmemorycontextaregenerallyassumedtoreflectdecision-makingprocesseswhentranslatingtherecogni-tionevaluationintoaresponse(Flecketal.,2006).Astrongeractivationofthisareabyconcretethanbyabstractwordshasbeendescribedinoneearlystudy(D'Espositoetal.,1997).Asisthecasefortheotheractivationsdescribedbefore,wecannotruleoutthepossibilitythatcommonactivationinthisareaduringretrievalofconcretewordsandduringonlineprocessingofconcretewordsintheencodingperiodreflectsdifferentcognitiveprocessesthatarenotfunctionallylinked.Anotherhintatabrainregioninvolvedinthememoryconcretenesseffectcomesfromthecorrelationofbrainactivitywiththebehavioraldata.Subjectsdisplayingalargerconcretenesseffectshowedastrongeractivationintheleftanteriorfusiformgyrusandthelefthippocampuswhencorrectlyidentifyinglearnedwords.Theleftmiddleandanteriorfusiformgyrushasbeenrepeatedlyreportedtobeassociatedwiththeretrievalofvisualobjectinformation(WheelerandBuckner,2003;Priceetal.,2003ratherthanwithimmediateobjectperception.Itisalsomorestronglyactivatedduringtherecollectionofstudiedpicturesascomparedtostudiedwords,evenwhenthetestitemsarewordsWoodruffetal.,2005;WheelerandBuckner,2004).Althoughtheactivationfoundinourstudyliesevenmoreanteriorwithinthefusiformgyrusthaninmostofthesestudies,weassumeittobeacorrelateoftheretrievalofvisualinformation.Thisfindingcanbeinterpretedinaccordancewithbothcontext-availabilitytheoryanddual-codingtheory.Ontheonehand,itshowsthattheretrievalofcontextualinformationisimportantfortheconcretenesseffect.Ontheotherhand,thenatureofthisinformationseemstobeprimarilyvisualaspredictedbydual-codingtheory.Thefindingofaconcretenesseffectinbrainactivationduringrecognition,butnotduringencoding,mayresultfromdifferentmechanisms.Oneexplanationissimplythatofstatisticalpower:duringrecognition,twiceasmanyeventscouldbeanalysedthanduringencoding.Anotherreasoncouldbethedifferenttaskdemands:theintentionallearninginstructionundertheencodingconditionmayhaveledtohighinter-individualvariabilityduetoindividualencodingstrategies.Thesamereasonsmightexplainthelackofsignificantmedio-temporalactivationswhichiscommonlyfoundasasubsequentmemoryeffect.Arepetitionoftheexperimentwithanincidentallearningconditionmightbeinstrumental.Athirdreasonmightbethatdifferentprocessesareactivatedbytheencodingtaskandtherecognitiontask.Sincetheparietalareasforwhichwefindtheconcretenesseffectareareasknowntodealwithitemidentification(Weisetal.,2004)theymightbemoreengagedunderarecognitiontaskthanduringanencodingtask.Inconclusion,ourfindingssuggestthattheanteriorbilateralprecuneustogetherwithlefthemisphericregionsincludingtheleftinferiorparietalcortex,leftanteriorfusiformgyrusandthelefthippocampusareinvolvedinthememoryconcretenesseffect.Studiesfocussingontheinteractionoftheseareasmightsupplyuswithimportantinsightsinthemechanismsofmemoryretrieval.ReferencesBaschek,I.L.,Bredenkamp,J.,Oehrle,B.,Wippich,W.,1994.BestimmungderBildhaftigkeit,KonkretheitundderBedeutungshaltigkeitvon800Substantiven.In:Hager,W.,Hasselhorn,M.(Eds.),HandbuchdeutschspachigerWortnormen.Hogrefe,Göttingen.Binder,J.R.,Westbury,C.F.,McKiernan,K.A.,Possing,E.T.,Medler,D.A.,2005.Distinctbrainsystemsforprocessingconcreteandabstractconcepts.J.Cogn.Neurosci.17,905Bleasdale,F.A.,1987.Concreteness-dependentassociativepriming:sepa-ratelexicalorganizationforconcreteandabstractwords.J.Exp.Psychol.13,582Cabeza,R.,Dolcos,F.,Graham,R.,Nyberg,L.,2002.Similaritiesanddifferencesintheneuralcorrelatesofepisodicmemoryretrievalandworkingmemory.Neuroimage16,317Cavanna,A.E.,Trimble,M.R.,2006.Theprecuneus:areviewofitsfunctionalanatomyandbehaviouralcorrelates.Brain129,564D'Esposito,M.,Detre,J.A.,Aguirre,G.K.,Stallcup,M.,Alsop,D.C.,Tippet,L.J.,Farah,M.J.,1997.AfunctionalMRIstudyofmentalimagegeneration.Neuropsychologia35,725Fiebach,C.J.,Friederici,A.D.,2004.Processingconcretewords:fMRIevidenceagainstaspecificright-hemisphereinvolvement.Neuropsy-chologia.42,62Fiebach,C.J.,Friederici,A.D.,Muller,K.,vonCramon,D.Y.,Hernandez,A.E.,2003.Distinctbrainrepresentationsforearlyandlatelearnedwords.Neuroimage19,1627Fleck,M.S.,Daselaar,S.M.,Dobbins,I.G.,Cabeza,R.,2006.Roleofprefrontalandanteriorcingulateregionsindecision-makingprocessessharedbymemoryandnonmemorytasks.CerebCortex.(Jan.12).Fletcher,P.C.,Shallice,T.,Frith,C.D.,Frackowiak,R.S.J.,Dolan,R.J.,1996.Brainactivityduringmemoryretrieval.Theinfluenceofimageryandsemanticcuing.Brain119,1587Friederici,A.D.,Ruschemeyer,S.A.,Hahne,A.,Fiebach,C.J.,2003.Theroleofleftinferiorfrontalandsuperiortemporalcortexinsentencecomprehension:localizingsyntacticandsemanticprocesses.CerebCortex13,170Henson,R.N.A.,Rugg,M.D.,Shallice,T.,Josephs,O.,Dolan,R.J.,1999.Recollectionandfamiliarityinrecognitionmemory:anevent-relatedfunctionalmagneticresonanceimagingstudy.J.Neuroscience19,Henson,R.N.,Hornberger,M.,Rugg,M.D.,2005.Furtherdissociatingtheprocessesinvolvedinrecognitionmemory:anfMRIstudy.J.Cogn.Neurosci.17,1058Jessen,F.,Heun,R.,Erb,M.,Granath,D.O.,Klose,U.,Papassotiropoulos,A.,Grodd,W.,2000.Theconcretenesseffect:evidencefordualcodingandcontextavailability.BrainLang7,103112.Kiehl,K.A.,Liddle,P.F.,Smith,A.M.,Mendrek,A.,Forster,B.B.,Hare,R.D.,1999.Neuralpathwaysinvolvedintheprocessingofconcreteandabstractwords.Hum.BrainMapp.7,225Klaver,P.,Fell,J.,Dietl,T.,Schur,S.,Schaller,C.,Elger,C.E.,Fernandez,G.,2005.Wordimageabilityaffectsthehippocampusinrecognitionmemory.Hippocampus15,704Lundstrom,B.N.,Petersson,K.M.,Andersson,J.,Johansson,M.,Fransson,P.,Ingvar,M.,2003.Isolatingtheretrievalofimaginedpicturesduringepisodicmemory:activationoftheleftprecuneusandleftprefrontalcortex.Neuroimage20,1934Mellet,E.,Tzourio,N.,Denis,M.,Mazoyer,B.,1998.Corticalanatomyofmentalimageryofconcretenounsbasedontheirdictionarydefinition.Neuroreport9,803Noppeney,U.,Price,C.J.,2004.Retrievalofabstractsemantics.Neuro-image22,164Paivio,A.,1986.MentalRepresentation:Adualcodingapproach.OxfordUniv.Press,London.Perani,D.,Cappa,S.F.,Schnur,T.,Tettamanti,M.,Collina,S.,Rosa,M.M.,Fazio,F.,1999.Theneuralcorrelatesofverbandnounprocessing.APETstudy.Brain122,2337Price,C.J.,Noppeney,U.,Phillips,J.,2003.Howisthefusiformgyrusrelatedtocategory-specificity?CognitiveNeuropsychology20,Ross,J.S.,Tkach,J.,Ruggieri,P.M.,Lieber,M.,Lapresto,E.,2003.Themind'seye:functionalMRimagingevaluationofgolfmotorimagery.AJNRAmJNeuroradiol.24,1036Schwanenflugel,P.J.,Akin,C.,Luh,W.,1991.ContextavailabilityandtheK.Fliessbachetal./NeuroImage32(2006)1413