An associative analysis of object memory

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ContentslistsavailableatScienceDirect

Behavioural

Brain

Research

j o ur na l h o me p a g e :w w w . e l s e v i e r . c o m / l o c a t e / b b r

Research

report

An

associative

analysis

of

object

memory

Jasper

Robinson

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Charlotte

Bonardi

SchoolofPsychology,TheUniversityofNottingham,NG72RD,England,UK

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•SynopsisgivenofmodelofassociativememorywhoseoriginisasatheoryofPavlovianconditioning.

•Objectrecognitiontasksareexplicableintermsoftheassociativememorymodel.

•Experimentalpredictionsfromtheassociativemodelarefoundtobesupported.

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Articlehistory:

Received30June2014

Receivedinrevisedform27October2014 Accepted29October2014

Availableonline13November2014

Keywords:

Associativelearning Discrimination Objectrecognition Pavlovianconditioning Priming

Recognitionmemory

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Differentaspectsofrecognitionmemoryinrodentsarecommonlyassessedusingvariantsofthe sponta-neousobjectrecognitionprocedureinwhichanimalsexploreobjectsthatdifferintermsoftheirnovelty, recency,orwheretheyhavepreviouslybeenpresented.Thepresentarticledescribesthreestandard variantsofthisprocedure,andoutlinesatheoryofassociativelearning,SOP[1]whichcanofferan expla-nationofperformanceonallthreetypesoftask.Theimplicationsofthisfortheoreticalinterpretations ofrecognitionmemoryandtheproceduresusedtoexploreitarediscussed.

1. Introduction

Wemaytakerecognitionmemoryasbeingthediscrimination betweennovelandfamiliarevents[2–4].Ithasbeenpopularto examinerecognitionmemoryinrodentsbycapitalisingontheir tendencytoapproachandexplorenovelorunexpectedobjectsin preferencetofamiliarorexpectedobjects[5,6].Systematic varia-tionsinthisprocedurehaveencouragedparticularaccountsofthe psychologicalprocessesunderlyingobjectrecognition:Ennaceur &Delacour[7](seealso[8,9])parsimoniouslydescribememoryas thehabituationofanapproachresponsetowardsanobjectwith increasedexposure;AggletonandBrown[10]maintainthatitis

Abbreviations:A1,primarystateofstimuluselementactivityinSOP;A2,primed orsecondarystateofactivityinSOP;CS,conditionedstimulusorsignal;US, uncon-ditionedstimulusoroutcome.

∗_{Corresponding}_author._Tel.:₊₄₄₁₁₅_9515322;_fax:₊₄₄₁₁₅_9515324. E-mailaddress:jasper.robinson@nottingham.ac.uk(J.Robinson).

URL:http://www.jasperrobinson.wordpress.com/(J.Robinson).

basedonasenseoffamiliaritytowardsanobjectthatisbuiltup throughexposuretoit(seealso[2,11]);Cowell,Bussey,and Sak-sida[12]describeamulti-layerconnectionistnetworkthatallows recognitiontooccurasin thenatural courseofthebuildingof stimulusrepresentationsandseveralauthorshavesuggestedthat rodents’recognitionmemoryrepresentsarelativelysophisticated formofmnemonicprocess[13,14].

Inthisreportwedescribeanalternativepsychologicalaccount ofrecognitionmemory,whichisbasedonBrandon,Vogel,& Wag-ner’smodel[15],SOP(StandardOperatingProcedures;[16–18]). SOPisprimarilyamodelofassociativelearning,butunlikesome others[19]incorporatesaconceptualisationofmemory.Weargue herethatthisfeatureofSOPallowsittoaccommodatemuchofwhat isknownaboutrodents’objectrecognitionandshowthatithas generatedpredictionsthathavebeenexperimentallysupported. SOPhasproducedsuccessfulaccountsofmanyphenomena(e.g., habituation[3,20,21],associativelearning,discriminationlearning) andifitsaccountofobject recognitionwereaccepted,itwould strengthen its positionasa general-purposemodel of adaptive behaviour.

http://dx.doi.org/10.1016/j.bbr.2014.10.046

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Fig.1. Objectrecognitionexperimentaldesigns.Experimentaldesignsforthree, keytypesofobjectrecognitionprocedure:spontaneousobjectrecognition,relative recencyandobject-in-context.PandQrefertodistinctlydifferentobjects;xand yrefertodistinctlydifferentcontexts.Theinequalitysignsindicatetheobjectthat elicitsthemostapproachbehaviour.

2. Objectrecognitioninnon-humananimals

2.1. Generalproceduralfeaturesandexperimentalconsiderations

Spontaneous object recognition [7,22–25], relative recency

[13,26–31]andobject-in-context[32–38]aretermsgiventothree ofthemostpopularproceduresforlookingatobjectmemoryin rodents(seeFig.1).Wedescribeeachinturn,beforediscussingan associativemodelofmemory,SOP,[15]thatcanprovidea satis-factoryexplanationofperformanceonthesethreetasks,andalso generatenovel,testablepredictions.

Allthreeproceduresinvolvetheplacementofarodentinoneor moreexperimentalcontextsalongwithoneormoreobjects;unlike matching-andnon-matching-to-sampleproceduresforstudying memory[39–41],foodreinforcementisnotusedinthesetasks. Experimental contexts vary in complexity, from being a single undecoratedwoodenboxtopairsofcontextsdifferentiatedintheir floors and/orwalls. Theexperimentalobjects areoften domes-ticitems(bottles,vases,etc.)thatareselectedtobedifficultfor rodentstoknock over, chewor situpon,behaviours thatcould easilycontaminatethemeasuredbehaviour.Thethreetasksdiffer principallyinthepreexposurethatrodentsreceive(whichisfully describedbelow).Forexample,inspontaneousobjectrecognition oneobject,P,ispreexposed.Inallthreetasks,testperformance involvesthesimultaneouspresentationofapairofdifferentobjects (PandQ),whichhavebeentreateddifferentlyearlierinthe pro-cedure(butsee[42]).Theexperimenterwillmeasuredifferences intheamounts ofbehaviourdirected towardsobjectsPand Q. Thismayeitherbespecificexploratoryresponses[32,33]orentry intonotionalzonesthatsurroundeachobject[31,43,44].In spon-taneousobjectrecognition,approachtoPisdepressedrelativeto Qontest[26,33]anddecreasesoverthecourseofpre-exposure

[20,45].

InterpretationofadifferenceinbehaviourtowardsobjectsPand Qrequiresappropriateexperimentalmanagement.Forexample,it isessentialtocounterbalancetheobjectsservingasPandQ(e.g., halfoftherodentshaveabottleasPandavaseasQ;theremaining rodentsreceivethereversearrangement)aswellastheirpositions withinthecontext(e.g.,halfoftherodentsreceiveobjectPonthe leftofobjectQ;theremainingrodentsreceivethereverse arrange-ment).Itisalsonecessarytoensurethatthetwoobjectsdonot differintheirmarking(e.g.,byodourcues),whichmaybeachieved eitherbycleaningorreplacingthemafteruse.

2.2. Threetypesofobjectrecognitiontask

In a spontaneous object recognition experiment [7,22–25], rodentsreceiveapre-exposuretrialwithobjectPbeforetesting withPandanovelobject,Q.QisapproachedinpreferencetoPon

testing.Typicallytwoversionsofasingleobject(here,P)are pre-exposedsothatthearrangementofobjectsinthecontextduring preexposurematchesthatduringtesting.Justasindelayed non-matchingtosample [46–49],in spontaneousobject recognition theintervalbetweenpre-exposureandtestingcanbeextendedto reducetestdiscrimination[50–52].

Thistemporal dynamic ofthe intervalbetween preexposure andtestisexplicitlymanipulatedintherelativerecencyprocedure

[13,26–31].Heretwopre-exposuretrialsprecedetesting:theﬁrst iswithP; thesecondwithQ.Ontest,rodentsapproachPmore thanQ,demonstratingbettermemoryofthemorerecently pre-sentedQ.Theinterval betweenthetwopre-exposuretrialsand theintervalbetweenthesecondpre-exposuretrialandtestwill emergelaterasimportantconsiderationsintheevaluationofthe associativeanalysisofobjectmemory.

Liketherelativerecencyprocedure,theobject-in-context pro-cedureinvolvestheseparatepre-exposureofbothobjectsPandQ beforethetest.Thedifferenceisthatpre-exposuretoeachobject occursinadistinctlydifferentcontext:ObjectPincontextxand objectQincontexty.GreaterapproachtowardsQthanPisfound whentestingoccursincontextx[32–38];and,ofcourse,testing maybegivenincontextyinwhichapproach isbiasedtowards P.Theparticularsequenceofpre-exposuretrials(xPbeforeyQor thereverse)mayconstitutearelativerecencymanipulationand itsimplicationsfor ourevaluation ofSOP areconsideredbelow (Section3.4.3).

2.3. Brainareasassociatedwiththesethreetypesofobject recognition

Althoughourreportis intendedtoconsidera psychological-levelofanalysisofrecognitionmemoryitisworthwhiletoconsider brain areas that are associated with the three forms of object recognition.Evidenceoftheimportanceoftheperirhinalcortex inspontaneous objectrecognitionis excellentin thatthere are manyexamplesofitsinvolvement(primarilyfromlesionstudies inrats)fromavarietyoflabs(e.g.,[22,23,28,37,45,49,53,54])and, asfarasweareaware,therearenoclaimsofnullﬁndings.There isalsosomeevidenceofinvolvementofprefrontalcorticalregions

[28]butmixedfindingsofinvolvementofthehippocampus(e.g., withdeficitsreportedinsomelabs,e.g.,[23,50],butnotinothers, e.g.,[35,38,55]).Fewerbrainregionshavebeenexaminedin rel-ativerecencyproceduresbutthereisabundantevidenceforthe involvementofspecificregionsoftheprefrontalcortexinrats(e.g.,

[27,28,56,13,57])and,againoftheperirhinalcortexandits connec-tionswiththeprefrontalcortex(e.g.,[28,13]).Object-in-context learninghasbeendemonstratedtobeaffectedbymanipulations ofthehippocampus(e.g.,[35,38,55],seealso[58]forevidenceof hippocampalinvolvementinanaudio-visualanalogueof object-in-contextlearning)andtheprefrontalcortex(e.g.,[28,36]).

3. TheSOPmodelofassociativememory

3.1. Stimulusrepresentation

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Fig.2. Activitytransitionsofstimuluselements.

ThisﬁgureisastillfromamoviethatisembeddedinthePDFversionofthis manuscript(seeAppendixA).Themovierepresentsthesequenceofactivity tran-sitionstatesinBrandonetal.’sSOPmodel.Threestimuluselementsareinitiallyin aninactivestate.Clickingthe“Activate”buttonisanalogoustothepresentationof astimulustoanorganism,suchasthepresentationofatonetoarat.Theratwill typicallyshowastrongorientingresponsetothesourceofthetone(representedas, “?!”),correspondingtothestimuluselements’promotiontotheirA1statesof activ-ity.Theelementsarenext“primed”(i.e.,theyenteraninferiorA2stateofactivity) wheretheyprovokeweakerorientingresponses.Finally,theelementsre-entertheir inactivestateswheretheydonotprovokestimulus-speciﬁcbehaviour.For compu-tationalreasons,Brandonetal.conceiveofstimulusrepresentationsascomprising muchlargerpopulationsofelementsthanthis;nonethelessthesequenceinwhich thestimuluselementspassthroughthevariousactivationstatesisidentical,and ele-mentscannotpassdirectlyfromA2backtoA1.Thuspresentationofthetone(i.e., clicking“Activate”)whenitselementsareintheirA2statedoesnotpromotethem intotheirA1state:EntryintoA1statemustcomedirectlyfromtheinactivestate.

tonerepresentationwouldbecomeassociatedwiththe represen-tationalelementsthatcodeforthefood(withtheirowndistinctive codingpropertiesrelatingtoitssmell,texture,etc.)Presentation ofthetonecouldproducefood-relatedrespondingbyactivationof thefoodstimuluselementsviatheseinter-elementassociations. Moreover,presentationofaphysicallysimilar,butdiscriminably different,tone(e.g.,onehavinga1.8Hzpitchwithanamplitude, again,of 65dB SPL) couldalso produceresponding, albeit at a reducedlevel,totheextentthatitsharedoneormorestimulus elementswiththetoneusedintraining[59–61].

3.2. Activitystates,theirtransitionsandbehaviour

Hebb[62]describedlearningprinciplesinwhichcellassemblies (whicharenotionallyidenticaltostimuluselementsinSOP)are ineitheractiveorinactivestates.Coincidentperiodsofactivityin cellassemblieswouldpromotetheformationofexcitatory associa-tions.However,Hebb’ssystemfailstopredicthallmarkassociative learningphenomenasuchasblockingandrelativevalidity[63,64]. LikeHebb’smodel,SOPsupposesthatconcurrentlyactivestimulus elementswillsupportassociationformation(thiswillbeoutlined belowinSection3.3)butsupposestheexistenceoftwoqualitatively differentformsofactivity.

Arepresentationofabrief,2.0-kHztone’sstimuluselements andtheirtransitionthroughSOP’sactivitystatesissummarisedin theHTMLmovieinFig.2.Thetone’selementsbegininthe inac-tivestateandtheywillnotelicitanybehaviour.ClickingtheAction buttoncorrespondstothepresentationofthetoneandthiswill promotethetone’selementsintotheirprimaryformofactivity(A1 state)inwhichtheywillelicitbehaviour.Oninitialpresentationof atone,theratwillelicitastrongorientingresponse[9],forexample towardstheloudspeakerandthisisrepresentedbythelargehazard sign,markedwith“?!”.Withsustainedorrepeatedpresentation, thetone’selementswillfadeintotheirsecondarystateofactivity (A2state)wheretheywillelicitweakerorienting,whichis repre-sentedbyasmallerhazardsignmarkedwith“?”.Elementsintheir A2statesarereferredtoasprimed.AftertheirperiodofA2activity, orpriming,theelementsdecaytotheirinactivestatesandnolonger elicitorienting.Threepointsarenotablehere:1.Themomentary

probabilityofeachelement’stransitionfromonestatetothenext neednotbeuniform.Thisallowselementsofasinglestimulusto inhabitdifferentactivitystatesatthesametime;2.Astimulus ele-mentisassumedtobeindivisible–itcannotinhabitmorethanone activitystatesimultaneously;3.ElementsmustpassintotheirA1 statesviatheirinactivestates,aswesawinthemovie:Theycannot movedirectlyfromA2toA1.Thus,forexample,asecond presenta-tionofthetonewhiletheelementsareintheirA2statesdoesnot returnthemtotheirA1states.

Brandonetal.describeasecond,associativerouteofprimingin SOP.Followingsuccessfulassociativelearning,forexampleinan appetitiveconditioningprocedure,atonesignalwillgenerateA2 activityinthefoodoutcome.Thatis,thepresentationofthetone generatesA1activityinitscentralrepresentation,whichprimesthe food’srepresentationdirectlyintotheA2stateviatheexcitatory associationbetweenthem.Onceprimed,thefoodrepresentation provokesconditionedresponding.SOP’sassociativeprimingallows ittoaccommodatemanylong-standingphenomenainanimal dis-criminationlearning,suchasblocking[64,65]andrelativevalidity

[63]–inkeepingwithothermodels[19,60,66].Associativepriming alsoallowsSOPtocorrectlyanticipatethatassociativelearningwill reachanasymptote,afeaturelackinginHebb’s[62]model.

3.3. SOP’srulesforassociationformation

Having outlined SOP’s transition characteristics for stimulus elementswe arein thepositiontounderstanditsfourrulesfor associativelearning.Therulesarestraightforwardandrepresented inFig.3:Excitatoryassociationswillbeformedbetween stimu-luselementswhoseelementsaresimultaneouslyintheirA1states (ﬁrstrule);inhibitoryassociationswillbeformedfromA1-state

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elementstoA2-stateelements(secondrule)butnoassociations willbereciprocated(thirdrule).Noassociativechangeswilloccur amongA2-stateelements(fourthrule).Futurepresentationsofa stimuluswillactivatetherepresentationofassociatedelements viaexcitatoryassociationsintotheirA2state;butinhibitory asso-ciationswillpreventthis,leavingtheelementsinactive.Wenext outlinecircumstancesinPavlovianconditionedexperimentswhere SOPassumestheseassociativechangestakeplace.

In standard Pavlovian conditioning in which, for example, rodentsreceiveabrieftonewhoseterminationiscoincidentalwith deliveryofafoodpellet(Tone→Food;e.g.,[67,68]),thepairingof thetoneandfoodwilltendtopromotetheirstimuluselementsinto theirA1statesandthiswillsupportexcitatoryconditioning.SOP predictsthatthebestconditionforsupportingassociativechange iswhenstimuluselementsarepairedsimultaneouslybutPavlovian conditioningprocedurestypicallyinvolvestheserialpairingofthe signal(orconditionedstimulus–CS)andoutcome(or uncondi-tionedstimulus–US).Thereasonsforthisaremerelypractical: Withserialsignal→outcome pairings,measurement of respon-dingtotheCSisfree ofcontaminationfromtheunconditioned responsestotheoutcome.However,speciallydesignedanalytical experimentshavefoundlearningaboutsimultaneouslypresented stimulitobesuperiortolearningaboutseriallypresentedstimuli

[69],theﬁndinganticipatedbySOP.

Aninhibitorysignalforanoutcome(aninhibitor)willnot pro-ducedistinctbehaviourwhentesteddirectlyinthewaythatan excitatorysignalwill.Instead,inhibitionisinferredfromtheresults ofapairofindirecttestsforinhibition[70].In“retardationtests”, theinhibitor servesas a standard Pavloviansignal forthe out-comefollowinginhibitiontraining.Theacquisitionof(excitatory) conditioned responding to the inhibitor is slow relative to an appropriatecontrolcondition.The“summationtest”involvesthe superimpositionoftheinhibitoronapreviouslyestablished exci-torforthesameoutcome.Theinhibitorreducestheconditioned responsethatisotherwiseelicitedbytheexcitor.Retardationand summationtestscomplementeachotherandmanyarguethatboth mustbepassedtoclaimthatastimulusisatrueinhibitor[71].

“Backwardconditioning”and“featurenegativetraining” proce-dureshavebothbeenfoundtoproduceinhibitionbyretardation andsummationtesting.A1-signalactivitycanbepairedwith A2-outcomeactivityinPavlovianconditioningwhenthe“outcome” precedes,ratherthanfollows,the“signal”(i.e.,outcome→signal pairings,or “backward conditioning”). Whentested after train-ingthesignal mayproducenegligible performance [72], which SOPwouldassumetobetheresultofamixtureofexcitatoryand inhibitorysignal-outcomelearningcausedbytheA1-signal activ-ity’sco-occurrencewiththeoutcome’selementsastheydecayfrom A1toA2activitystates.Withalterationsinexperimental param-eters,itispossibleforoutcome→signalpairingstoproducefull inhibitorylearninginwhichthesignalisfoundontesttosuppress activityintheoutcomerepresentation[72].HereSOPwillassume thatthereisgreaterco-occurrenceoftheoutcome’sA2stateand thesignal’sA1statethantheoutcome’sA1stateandthesignal’sA1 state.AcommonermethodforarrangingthepairingofA1-signal andA2-outcomeactivityisfeature-negativediscrimination train-ing[70,71,73].Heresomethirdstimulus,e.g.,alight,isestablished asasignalforfoodandthetoneandlightarepresentedasa com-pound,whichisnotreinforcedbyfooddelivery(i.e.Light→Food, [Tone+Light]→nothing).

There are important parallels between SOP and its better-knownrelative,theRescorlaandWagnermodel[19].TheRescorla and Wagner model describes the notional changes in associa-tive strength between the representations of a pair of events on any particular trial, by the expression, V=_˛ˇ(₋V). In particular,thechangeinassociativestrength(V)isproportional tothedifference in themaximum level of associative strength

(asymptote, ) and the sum total of each previous associative change(V)multipliedbytheproductofapairoflearning-rate parameters(˛andˇ)thatareassociatedwiththetwoeventsand where1≥˛>0and1≥ˇ>0.DuringPavlovianconditioning,each signalled outcomepresentationwill beless surprisingthanthe last;thisiscapturedbyincreasesinV,producingadeclineinthe term(−V),whichresultsinincreasinglysmallincrementsin V,yieldinganegativelyacceleratinglearningcurve.SOPshares this property,which is achieveddifferently through associative priming(Section3.3).Onthefirsttrialthesignalandoutcome’s conjointA1activitywillbegoodandthiswillincreaseexcitatory strengthbetweenthem.On thenexttrialthesignal’sexcitatory strengthwillprimetheoutcome.Theassociativeprimingwillbe weakonthesecondtrialbutitwillallowsomeoverlapofthe sig-nal’sA1elementsandtheoutcome’sA2elements(Fig.3).Outcome elementsthatarenotprimedwillbefreetoentertheirA1stateson thesecondtrialandthiswillproducesomeexcitation.Theratioof excitationtoinhibitionwilldecreaseasVincreasesoneachtrial andVwillreachasymptote()andatthispointchangesin exci-tationandinhibitionareequaloneachtrial.ThustheRescorlaand WagnermodelandSOPaccountforcompetitionforafixedquota ofassociativestrengthinthesamewayandthisprincipleextends tootherkeyassociativephenomenasuchasblocking[64,65],super conditioning[74]andrelativelyvalidity[63].SOPmaybeseenas a morecomplete modelthan Rescorlaand Wagner’sbecauseit operatesinrealtime[75,76]andanticipateslatentinhibitionand itscontextspecificity[77],someperceptuallearningphenomena

[78],andmodulationofUCSprocessing[76,79].

3.4. Decayprimingandobjectrecognition

Theconclusionsofthisandthefollowingsectionare summari-sedinFig.4.

Itmayalreadybeobviousthatthelearningprocessdescribed by SOP for Pavlovian conditioning (Sections 3.2 and 3.3) may applytootherstimuli,includingthoseusedinobjectrecognition experimentswithrodents.Althoughwemightconceiveofthe rep-resentationsofobjectsasbeingmorecomplexthanthoseofapure

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tone,andcomposedofelementscorrespondingtomultiplesensory domains,thesameprocessescanbeapplied.

3.4.1. Spontaneousobjectrecognition

Therodent’sinitialencounterwithobjectPduringspontaneous objectrecognitionwillgenerateA1activityintherepresentational elementsthatprovokestrongapproachbehaviour.Aftersometime this behaviour willweaken, correspondingto theobject-P ele-ments’entryintotheirA2state.Testpresentationduringthistime wouldresultinthestandardbiastowardsexplorationofthenovel object,Qbecauseitsrepresentationalelementscanpassfreelyfrom theirinactivestatestotheirA1stateswhereastheelementsofPthat arestillintheA2-statecannot.

3.4.2. Relativerecency

Wenotedabove(Section2.2)thatspontaneousobject recogni-tionperformanceworsenswhenaretentionintervalisinterpolated betweenthepre-exposureandtesting[50–52].OneofSOP’s expla-nationsof thisisthat longerretentionintervalsallowagreater proportionofP’selementstoreturnfromtheirA2totheir inac-tivestates.Thus,ontest,bothP’sandQ’sinactiveelementscan passdirectlytotheirA1stateswheretheycanelicitsimilar,strong levelsofapproach.Demonstrationsofrelativerecency[13,26–31]

receiveanidenticalexplanationfromSOP:Thepre-exposureofP andthenofQwillelicitA1activityintheirelementsthatwill,over time,decaytoA2andtheninactivestates.BecausePispre-exposed beforeQitispossibletoarrangefortestingwithPandQatatime whenP’selementstendtobeinactivebutQ’selementsremainin theirA2states.HereP’selementsarefreetoentertheirA1states wheretheyelicitstrongapproach;butmanyofQ’selementsmay remainintheirA2statesandonlyweakapproachiselicited.

3.4.3. Object-in-context

ThemostnaturalSOPaccountofobject-in-contextlearningis describedfullybelow(Section3.5.1)andreliesontheoperation ofassociationsbetweeneachcontextandtheobjectthathasbeen pre-exposedinit(i.e.,x→Pandy→Q).Testingincontextxwill primeobjectP’selementsbutnotobjectQ’s.Thusthepresenceof PandQontestinxwillallowQ’selementstoentertheirA1states fromtheirinactivestates,wheretheycanelicitrelativelystrong approach;butP’sprimedelementswillremainintheirA2state, unabletoelicitsuchresponding.

Althoughsuchassociative-primingprocessesseemplausible,it isimportantalsotoconsiderpossibledecay-primingprocessesin object-in-contextlearning.Thetemporalasymmetriesdescribed forrelativerecencyarealsopossibleinobject-in-contextlearning whenasingletrialofeachtypeisused:Heretherearetwo possi-blesequencesfortheobjectandcontextpre-exposures(i.e.,either xP,yQoryQ,xP).Ofcourse,thisispreciselythearrangementof objectpre-exposureinarelativerecencyexperiment,andsoSOP anticipatesthattheﬁrst-pre-exposedobjectwillprovokestrongest approach,basedondecaypriming.Theassociative-priming mech-anismpredictsgreaterapproachofQthanofPontestincontext x,inwhichitisunexpected.Thus,decay-andassociative-priming willopposeoneanother(i.e.,weakeningdiscrimination)butpullin thesamedirection(i.e.,enhancingdiscrimination)withtheyQ,xP pre-exposuresequence.Wehaverecentlyfoundevidenceofsuch interactionsbetweenassociativeanddecaypriming(Tam,Bonardi, &Robinson,reportunderreview).

Althoughdecayprimingappearstoinﬂuenceperformance in object-in-context learning, it cannot adequately account for it. Therearetwo reasonsfor this statement: First,in experiments inwhich onlya singlexPandyQtrialisgiven [33–38], object-in-contextlearning isdetectedwhen performanceoverthetwo possiblepre-exposuresequencesiscollapsed.Thatis,although dif-ferencesindecayprimingappeartooperate,theywillassistand

hinderdiscriminationperformanceinequalmeasureoverboth pre-exposuresequences.Thefactthattestdiscriminationissuccessful impliestheoperationofasecondprocessoverandabovedecay priming;second,itispossibletoarrangemultiplepre-exposure trialssothatforeachrat,onaverage,objectsPandQhavebeen presentedequallyrecentlybeforetesting.Thisisachievedby pre-sentingxPandyQpre-exposuresmultipletimes,e.g.,xP,yQ,yQ,xP forhalfofthesubjectsandyQ,xP,xP,yQfortheremainderandalso resultsinobject-in-contextlearning[32].

Thus,itappearsthatdecayprimingisrequiredtoexplain rela-tiverecencybutcannotaccommodateobject-in-contextlearning. Decayprimingcouldalsoexplainspontaneousobjectrecognition.

3.5. Associativeprimingandobjectrecognition

3.5.1. Spontaneousobjectrecognition

Brandonet al. anticipate a second, association-based source ofspontaneousobjectrecognition:Contextcuesenterinto excit-atoryassociationswithobjectP’srepresentationalelementsduring objectP’spre-exposure(see,e.g.,[18,21,43]).Thus,contextcues willgenerateA2activity(butnotA1activity)inobjectP’s repre-sentationalelementsontesting.Aswiththedecay-basedsource ofperformance,theassociativesourceisbasedontheelements forobjectAtendingtobeintheirA2states,whilethoseforobject QtendtobeintheirA1stateatthepointoftesting.Thusitseems thatbothassociativeanddecayprimingcouldsupportspontaneous objectrecognition.

3.5.2. Relativerecency

Inthecaseofrelativerecency,anysuchcontext→Passociation willbematchedbyacontext→Qassociationandsotest discrim-inationcannotobviouslybeaccountedforbyassociativepriming. However,non-reinforcementofasignalmayextinguishexcitatory learning[80,81]andfollowsSOP’srules(i.e.,thenon-reinforced signalwillelicitA2activityintheoutcome’srepresentationthat willgenerateinhibitoryassociativelearning).Thusanycontext→P associationcouldundergoextinctionduringthesubsequentpairing ofthecontext withQ,duringwhichP isabsent.Thus test per-formancecouldbebasedentirelyonassociativeprimingbecause, duringtesting,thecontextwillbebetterassociatedwithQthan withP.ThiswillproducebetterprimingofQthanofP,leadingtothe observeddifference:greaterapproachofPthanQ.However,studies showthatmultiplenon-reinforcedtrialsarenecessarytoachieve appreciableextinction[80,81]–unlikethesingletrialnecessaryfor relativerecency.Thus,althoughanassociativeprimingaccountof relativerecencyislogicallypossibleitisempiricallyimprobable, andthisindicatesdecayprimingasthesolesourceofperformance.

3.5.3. Object-in-context

Themostdirectevidencefortheoperationofcontext→object associativeprimingcomesfromobject-in-contexttasks[32–38]. Aswenotedabove(Section3.4.3),accountsofobject-in-context learningbasedondecayprimingareimplausibleandso,by elim-ination,theassociativeprimingaccountseemsthemostrealistic componentoftheSOPmodelavailabletoexplainperformance.

3.6. Conclusionsabouttherolesofdecayandassociativepriming inobjectrecognition

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parameters(timing,stimulusduration,etc.),wecouldmanipulate themixofdecayandassociativepriminginspontaneousobject recognition.Buttheunavoidableconclusionisthat,accordingto SOP’sanalysis,spontaneousobjectrecognitionisanimprecisetool andisunsuitableforunderstandingseparablepsychological pro-cesses.Themixedﬁndingsontheeffectsofhippocampuslesions onrats’spontaneousobjectrecognition(cf.[23,40,50]and[22,39]) maybeexplicableifitisassumed,say,thatassociativepriming isdependentonthehippocampusandismoreprominentinthe proceduresofthoseﬁndinglesioneffectsthanthosewhohavenot (cf.[18]).Thislogicappliestoothermanipulations,ofcourse:For example,extensionoftheretentionintervalbetweenpre-exposure andtestwillhaveadevastatingeffectonspontaneousobject recog-nitionthatislargelydependentondecaypriming,butonebased largelyonassociativeprimingwillbeunaffected.Butthediscussion hereimpliesthatrelativerecencyandobject-in-contextlearning arerelativelyselectivetoolsforexaminingdecayandassociative primingrespectively.

Spontaneousobjectrecognitionhasbeendescribedasaformof habituation(7],seealso,[8,9])–thatis,adeclineinthebehaviour thatiselicitedbyastimuluswhenitispresentedrepeatedlyorover alongperiodoftime.Inthecaseofspontaneousobjectrecognition thestimulusisobject,Pandthemeasuredresponseisapproach orexploratorybehaviour.Thedeclinein thisbehaviourmaybe assumedtooccurduringpreexposurebutismeasuredinthetest relativetoobjectQ.Thestimulusspeciﬁcityshownheremeetsakey featureofhabituation.Severalauthorshavenotedthathabituation canbeunderstoodastheresultofadeclineintheefﬁcacyofthe pathwaybetweenastimulusandresponse[82].Itisquitepossible thatsimple,stimulus-responsebasedadaptiveprocessmayoccur alongsidethoseanticipatedbySOP.Oneimplicationofthisisthat neuralmanipulationsmayaffectSOP-basedprocessesandspare stimulus-responsebasedprocesses(e.g.,[8,9,58]),orviceversa.

Sokolov([83],seealso[84,85])described amodel of habitu-ationin which thepresentationof a newstimuluswill leadto thedevelopmentofarepresentationofit.Prolongedorrepeated presentationofthestimuluswillfosterincreasingdetail ofthat representationuntilitisentirelyaccurate.Theprocessof repre-sentationalmodificationisassumedtobetheresultofamismatch inmemory–thatisthestimulusiscomparedwithsetsof stimu-lusrepresentationsinmemory.Whencomparisonfindsamatch, norepresentationalmodificationis required;when comparison failstofindamatchanewrepresentationisassembled(oraclose matchisimproved).Inanhabituationprocedure,improvementsin stimulusrepresentationwillbeassociatedwithdeclinesin uncon-ditionedresponse(i.e.,habituation).LikeSokolov’smodel,theSOP model[15]allowsfortheassemblyofstimulusrepresentations– whentheirelementsareconcurrentlyintheirA1states–butno additionalprocessofcomparisontakesplace.Rather,changesin responsivenesstorepeatedlypresentedstimuliarebasedsolelyon theprimingprinciplesoutlinedabove.

4. Evidenceofassociativeprocessesinobjectrecognition

WehaveseenthatSOPcanbeappliedtostandard demonstra-tionsofobjectrecognition.Ofcourse,themerefactthatthismodel ﬁtsthedatadoesnotdemandthatthemodelshouldbeaccepted. Wenextdescribesomeevidencefromanalyticalobjectrecognition experimentsthatmakeastrongercaseforthisposition.

4.1. Enhancedspontaneousobjectrecognitionwhenmultiple pre-exposuresarespaced

We saw that spontaneous object recognition test perfor-mancecouldbetheresultofobjectP’srepresentationalelements

Fig.5.Spacedandmassedpre-exposureillumination.SchematicofWhittand Robinson’s[44]multi-trialpre-exposureinspontaneousobjectrecognition.Rats werepresentedwithobjectPduringpre-exposure,whichwasonlyvisibleduring eight30-speriodsofilluminations–contextswereotherwisedarkened.Theperiods ofdarknessdifferedacrosstwoconditions,beingeither4-min(spacedcondition) or30-s(massedcondition).Subsequentdiscrimination(greaterapproachtoobject QthanobjectP)wassuperiorinthespacedconditionthaninthemassedcondition.

becomingprimedthroughamixofdecayandassociativepriming, whichmayvaryaccordingtothepreciseexperimental parame-ters(e.g.,thepre-exposure-testretentioninterval).Totheextent thatassociativeprimingisinvolvedintestperformance,itwillbe importanttomaximisethestrengthofthecontext→object associ-ationduringpre-exposure.Aswesawabove(Section3.3),learning aboutthecontext→objectrelationshipwilloccuronlywhenthe context’srepresentationalelementsareintheirA1states,andthe valenceofthislearning(i.e.,whetheritisexcitatoryorinhibitory) willdependontheactivitystateoftheobject’srepresentational elements:WhentheyareintheirA1statestheassociationwillbe strengthenedthroughadditionalexcitation,buttheassociationwill beweakenedbyinhibitionwhentheyareintheirA2states.

Suchweakeningofthecontext→objectassociationisexpected whentheobject,Phasbeenrecentlypresented,asaresultof decay-basedpriming.Severalauthorshavereportedthatwhenmultiple pre-exposurestoobjectParegiven,testperformanceisbetterwhen thesepre-exposures are relatively well-spaced(e.g., [20,44,86]) andwehaveunpublisheddemonstrationsofanalogouseffectsin humanparticipants’performanceonanauditoryrecognition mem-orytask.Thepre-exposurescheduleusedbyWhittandRobinsonis representedinFig.5.Toensurefullexperimentalcontrolover stim-ulusscheduling,objectsPandQwerepresentedinglasscylinders, renderingthementirelyvisualstimuli.Allratsreceivedeight,30-s periodsofilluminationduringasinglepre-exposuresession, dur-ingwhichtimetheyremainedinthecontext.ObjectPwouldonly havebeenvisibleduringtheseperiodsofillumination.Rats’test performancefollowing spacedpre-exposure,inwhich the inter-valbetweeneachilluminationperiodwas4min,wassuperiorto thatfollowingmassedpre-exposure,inwhichitwasonly30s.Our interpretationisthatanappreciableproportionoftheobjects’ rep-resentationalelementsreturnedtoinactivityduringthefour-min inter-illuminationperiodandwereavailabletoentertheirA1states onthesubsequentperiod,thussupportingtheformationofthe context→objectassociation.However,themassedpre-exposure trialsoccurredwhenP’selementsweremorelikelytobeprimed. Thiswillhaveproducedsomeinhibitoryx-Plearningthatwould acttooffsettheexcitatoryx-Plearninguponwhichperformance partlyrelies.

4.2. Decaypriminginrelativerecency

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Fig.6. Temporalmanipulationsinrelativerecency.Schematicofthetemporal manipulationsinpre-exposure-trialandretention-intervalspacingintwo relative-recencyexperiments.Ratsinbothexperimentsreceivedsequentialpre-exposure trialswithobjectsPandQbeforetestingwiththetwoobjects.Tametal.used aﬁve-minretentionintervalbetweenpre-exposuretoobjectQandtesting.The durationoftheintervalbetweenthetwopre-exposuretrialswaseither5minor 2h;discriminationwasbetterwiththelongerinterval.MitchellandLaiaconaﬁxed thepre-exposureinter-trialinterval(at1h)andmanipulatedtheretentioninterval. Testdiscriminationwasgoodatretentionintervalsof24horless,butwasabsent at72-hintervals.Note:MitchellandLaiaconaincludedadditionalintervals,which arenotsummarisedhere.

duration of the inter-trial intervals. For example, with a suffi-cientlyshortretention interval (i.e.,thetime betweenthefinal pre-exposureandtesting),theintervalbetweenpre-exposureto PandQbecomescrucialinensuringthatP’selementsarelargely inactivebytest.Tam,Robinson,Jennings,andBonardi[87]have confirmedthispredictionofSOPinadesignthatissummarisedin

Fig.6.Theypresentedratswithpairsofobjects,PandQ,witha five-minintervalbetweenQandthetest.Inoneconditiontheinterval betweenPandQwasalso5min,andinanother2h.The2-hP-Q intervalproducedmarkedlystrongerdiscriminationthanthe five-minP-Qinterval.Tametal.demonstratedthatthistime-related reductioninperformance wasnot ageneraldeficit,byshowing avariantofobject-in-contextlearningtoremainunaffectedbya similarmanipulationoftheintervalbetweentrainingandtest.Itis alsonotablethattheanalysisofobject-in-contextlearning(Section

3.5.1)anticipatesthisinsensitivitybecausetheassociativepriming onwhichitrelieswillbeunaffectedbychangesinthepassageof time.

Arelatedpredictionisthatrelativerecencyshouldalsobe abol-ishedbyanextensionoftheretention interval(i.e.,theinterval betweenthesecondpre-exposuretrialandtest).Whensufficiently long,theretentionintervalwillallowtheelementsofbothPand Qtobecomeinactivesothat,ontest,A1activityinbothmaybe generatedandsimilarlevelsofapproachelicited.Mitchelland Laia-cona[29]reportjustsuchafinding.Ratsinthreegroupsreceived pre-exposuretoobjectPbeforeobjectQ,whichwasseparatedby a1-hinterval.TestapproachofQwasgreaterthanPwhen test-ingoccurredimmediatelyafterthepre-exposuretoP,but with theinterpolationofa72-hretentionintervaltestperformancewas attenuated.However,onefeatureofMitchellandLaiacona’sresults isproblematicforSOP:Relativerecencydiscriminationwasseen alsoinagroupwitha24-hretentioninterval.Inordertoexplain thispatternofresultstheanalysisofrelativerecencyoutlinedin Section3.4.2needstoassumethatP’selementshavedecayedto inactivityat25h,butthatat24hQ’sremainlargelyprimedintheir A2states.Whilethisisnotimpossible,itcouldbeseenasa sur-prisingcoincidence;giventheirpotentialtheoreticalsignificance, MitchellandLaiacona’sfindingswouldbenefitfromconfirmation andfurtheranalysis.

Fig.7.Schematicofprimedobject-in-context.Schematicofanobject-in-context experiment(e.g.,Whitt,Haselgrove,&Robinson)inwhichthethreestagesofthe experimentoccurfromlefttoright.Theprocedurebeganwithratsreceiving pre-exposuretoobjectPincontextxandwithpre-exposuretoobjectQincontexty, asinthestandardobject-in-contexttask.Nextratswereplacedincontextx;no objectwaspresentbutthistreatmentshouldbesufﬁcienttoallowtheassociative primingofobjectP.Inthesubsequenttest,ratswerepresentedwithbothobjects, PandQ,butinathirdcontext,z,whichwasassociatedwithneitherobject.Ontest, ratsapproachedQinpreferencetoPdespitetestingnotoccurringinP’scontext,x. Performanceisconsistentwiththeprimingmechanisms.

4.3. Associativeprimingofobject-in-contextlearning

Thecurrentanalysisofobject-in-contextlearning(Section3.5.3; seeFig.3)reliesontheassociativeprimingofobjectPbythetest context,x.Thisprimingof Pusuallyoccurs duringtherodents’ placementincontextxattest.However,accordingtothe analy-sissuggestedhere,thisisnotnecessary:Theonlyrequirementis thatxisprimedatthetime thatxandyaretested.Inorderto examinethissuggestionWhittHaselgroveandRobinson[43]used theproceduresummarisedinFig.7.Exactlyasinastandard object-in-contextlearningtask,ratswereinitiallypresentedwithobject PincontextxandobjectQincontexty,toallowtheestablishment ofx→Pandy→Qassociations.Inasubsequentstageratswere placedincontextx,butthiscontainednoobjects.Thisstagewas intendedtoassociativelyactivateobjectP’srepresentation,andthis primingwasassumedtoremainappreciableovertheshorttime beforetesting.Unlikestandardobject-in-contextlearning,testing withobjectsPandQoccurredinathirdcontext(e.g.,z)inwhich noobjectshadbeenexperienced.Despitethischangeinprocedure, andconsistentwithSOP,ratsapproachwasbiasedtowardsobject QrelativetoobjectP.

5. Discussion

Wehaveattemptedtoapplytheassociativemodelofmemory, SOP [16–18] to three representative forms of object recogni-tion that are popular procedures in experimental psychology and behavioural neuroscience. In considering its dynamic pro-cesses(decayandassociativepriming)anditsrulesforassociation formation,SOP produced asatisfactory accountofobject mem-ory. Experimental evidence [20,43,44,88] largely, though not universally (Section 4.2) supported SOP’s account’s of object recognition.

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ahigherformoftemporalmemory(e.g.,[13]).Thereisnothingin theprecedingdiscussiontoinformonthestatusoftheseintriguing andimportantpossibilitiesbuttheyareprobablymorecomplex explanationsthatarerequiredtoexplainavailableﬁndings.More troublingforsuchaccountsisthattheevidencedescribedhere sup-portsdirectpredictionsfromSOP.Itispossibleofcoursethatthese ﬁndingscouldalsobeinterpretedintermsofmoresophisticated memorysystems,thoughitisuncleartoushowthiscouldbedone anditis probablyunnecessarytodo so.Beingbasedonalarge bodyofexperimentalevidencefromthestudyofhabituationand Pavlovianconditioning,SOPcanbeusedtodeliverseveraltestable areasofexperimentationthatcouldfurtherevaluatethisaccount ofrecognitionmemory.

Disclosurestatement

Neitherauthorisawareofanyconﬂictofinterestcreated asso-ciatedwiththisreport.

Acknowledgements

TheauthorsthankDavidSandersonandEricTamforhelpful discussion.

AppendixA. Supplementarydata

Supplementarymaterialrelatedtothisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.bbr.2014.10.046.

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