Relative recency influences object in context memory

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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

Relative

recency

inﬂuences

object-in-context

memory

Shu

K.E.

Tam

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_Charlotte

_Bonardi

∗

_,

_Jasper

_Robinson

∗

SchoolofPsychology,UniversityofNottingham,UniversityPark,NottinghamNG72RD,UnitedKingdom

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•Resultsofobject-in-contextexperimentscanbeinﬂuencedbyrelativerecency.

•Datafromtwoexperimentspresentedsupportingthissuggestion.

•Thismaycomplicateinterpretationofresultsofobject-in-contextexperiments.

•Recommendationsaremadeonhowtoaddressthis.

•Resultsconsistentwithanassociativeaccountofrecognitionmemory.

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Articlehistory:

Received10October2014

Receivedinrevisedform5December2014 Accepted9December2014

Availableonline26December2014

Keywords:

Associativelearning Discrimination Objectrecognition Pavlovianconditioning Priming

Recognitionmemory

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Intwoexperimentsratsreceivedtrainingonanobject-in-context(OIC)task,inwhichtheyreceived preexposuretoobjectAincontextx,followedbyexposuretoobjectBincontexty.Inasubsequent testbothAandBarepresentedineithercontextxorcontexty.Usuallymoreexplorationisseenof theobjectthathasnotpreviouslybeenpairedwiththetestcontext,aneffectattributedtotheability torememberwhereanobjectwasencountered.However,inthetypicalversionofthistask,objectA

hasalsobeenencounteredlessrecentlythanobjectBattest.Thisispreciselythearrangementintests of‘relativelyrecency’(RR),inwhichmoreremotelypresentedobjectsareexploredmorethanobjects experiencedmorerecently.RRcouldcontaminateperformanceontheOICtask,byenhancingtheOIC effectwhenanimalsaretestedincontexty,andmaskingitwhenthetestisincontextx.Thispossibility wasexaminedintwoexperiments,andevidenceforsuperiorperformanceincontextywasobtained. Theimplicationsofthisfortheoreticalinterpretationsofrecognitionmemoryandtheproceduresused toexploreitarediscussed.

1. Introduction

Thephenomenonofspontaneousobjectrecognition(SOR)—the observationthatanimalsshowapreferenceforexploringanovel object rather than one that has been previously encountered

Abbreviations: OIC,object-in-context;RR,relativerecency;SOR,spontaneous objectrecognition.

∗Correspondingauthors.Tel.:+441159515218;fax:+441159515324.

E-mailaddresses:[email protected](S.K.E.Tam), [email protected](C.Bonardi), [email protected](J.Robinson).

URLs:http://www.eye.ox.ac.uk/team/research-scientists/shu-tam(S.K.E.Tam), http://www.nottingham.ac.uk/psychology/people/charlotte.bonardi(C.Bonardi), http://jasperrobinson.wordpress.com(J.Robinson).

1 _Now_at:_Nufﬁeld_Laboratory_of_{Ophthalmology,}_University_of_Oxford,_Level_5–6

WestWing,JohnRadcliffeHospital,HeadleyWay,OxfordOX39DU,UnitedKingdom. Tel.:+447854596500

[1–3]—underliesavarietyoftasksdesignedtoexaminememory processes in ratsand mice. One version of this, the object-in-context(OIC)task,isusedtoassessrodents’abilitytoremember

wheretheyhaveencounteredaspeciﬁcobject.Inonetypical vari-antofthistasktherodentisallowedﬁrsttofreelyexploreonetype ofobject,A,inonecontext,x,andsubsequentlyadifferenttypeof object,B,inanothercontext,y(seeFig.1).Eachcontext-object pair-ingusuallyconsistsofasingletrial.Afteradelay,atestwithobjects

AandBisgiveninoneorotherofthetwocontexts.Itistypically reportedthatnormalanimalsshowapreferencefortheobjectthat hasnotbeenencounteredinthetestcontext[4–12].Ithasbeen pro-posedthatthistaskrelatestothe‘where’componentofepisodic memory(e.g.,[11,12]),contextmemory(e.g.,[6]),recollection(e.g.,

[8])or,moregenerally,contextualprocessing[7,9,10].

AnothervariantoftheSORprocedure,therelativerecency(RR) task,isdesignedtoevaluatelearningaboutwhenanobjectwas experienced, by examining the animal’s ability to discriminate objectsbasedonhowlongagotheyhavebeenencountered.Here

http://dx.doi.org/10.1016/j.bbr.2014.12.024

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Fig.1. DesignofExperiment1andexampleofspeciﬁcobjectsandcontextspresentedinthesamplephasesofanOICrecognitiontrial.Aratisallowedtofreelyexploreone typeofobject(A)inonevisualcontext(x),andsubsequently,adifferenttypeofobject(B)inadifferentvisualcontext(y).Followingthesetwosamplephasesanimalsare givenachoicebetweenAandB,eitherinthelessrecentcontextx,orinthemorerecentcontexty.NotethatobjectAhasbeenencounteredearlierthanobjectB,andthus, atthetimeoftest,thememorytraceofobjectAwouldberelativelyweakerthanthatofobjectB.

theratisallowedtofreelyexploreonetypeofobject,A,and subse-quentlyadifferenttypeofobject,B,inthesameapparatus.Aftera delay,theanimalreceivesatestwiththeobjectsAandBpresented simultaneously[13–18].AnimalsshowapreferenceforobjectA, theobject thathasbeen encounteredearlier in theseries. Rel-ativerecencyhasbeendescribed asaformoftemporalmemory

inwhicheventsarerememberedinsequencethrougha higher-ordermnemonicfunction(e.g.,[13,14]).Thisdescriptionimpliesthat themechanismunderlyingRRislikelytobequitedistinctfrom thatresponsibleforOIClearning—indeedthelearningmechanisms involvedintheOICandRRversionsofthetaskareregardedas independent[19].

ThesuggestionthatRRandOICtasksrelyonindependent mech-anisms has, however, been challenged. For example, the most obviousanalysisofSOR(e.g.,[1–3])isthatexposuretoobjectA

leavesamemorytracethatispresentduringthetest,butabsent forthenewobject,B[18,20–23].PerformanceonRRtaskscanbe explainedinsimilarterms,byarguingthatthepreferenceforthe lessrecentAstemsfromitsmemorytracebeingweakerthanthat ofthemorerecentB.Moreover,asthedelaybetweenthesample trialsandtestingincreases,thedifferenceinpreferencebetween

AandBdeclines[18].Thismaybeunderstoodbyassumingthat thedifferenceinthetracestrengthofAandBisgreatestatshort delayswhenA’smemorytracehashadanopportunitytodecaybut

B’sremainsactive;asthedelayincreases,thememorytracesfor bothobjectswilleventuallydeclinetosomenegligiblevalue(for discussionsee,e.g.,[23,24]).Foreaseofexposition,wedescribe thedeclineinmemoryperformanceovertimeas‘decay’thoughwe acknowledgeherethatitmightbetheresultofamoreactive pro-cessofinterference(see,e.g.,[25]).Thatis,thememorytraceofthe targetstimulusmaybesupplantedbytheaccumulatedmemory tracesofinterferingstimulithatarepresentduringtheretention interval.Interferingstimulimaybeexplicitlyaddedbythe experi-menter(see,e.g.,[25,26])butevenwhentheyarenot,non-speciﬁc eventsinthelaboratorymaycreatethesameeffect(see,e.g.,[27]). Analternative,butrelated,analysisofSORmaintainsthat appa-ratuscuesenterintoanexcitatoryassociationwiththepre-exposed

A—theprocessassumedtounderliePavlovianconditioning.Attest, theexcitatoryassociationactivatesthememoryofthepre-exposed object,reducingthedegreetowhichitisexplored.Incontrastthe novelB,notbeingassociatedwiththeapparatuscues,isunexpected inthatapparatus; thusitsmemoryis notactivatedand normal explorationismaintained(e.g.,[20,28–30]).Thesameexplanation

canbeusedtoexplainOIClearning:Althoughbothobjectswill becomeassociatedwiththeirrespectivecontexts,onlythe mem-oryoftheobjectthathasbeenpreviouslyencounteredinthetest contextwillbesubjecttothisassociativeactivation,andthisiswhy itisexploredlessthanthealternativeobject.

ThisviewassumesthatwhileRRdependsondifferentialdecay ofthememorytrace(cf.[15–17]),OICstemsfromdifferencesin associativeactivationofthememorytrace[18,20–23,28–30],and both processesmaycontributetoSORperformance. This analy-sisofperformanceonbothOICandRRtasksintermsofthesame underlyingmechanismraisesthepossibilitythattheymight inter-act.Forexample,intheOICprocedureoriginallydescribedbyDix andAggleton[5],animalsreceivedtwoexposurestoeachofthe objects,AandB,intheirrespectivecontextsinadouble alterna-tionprocedure(A,B,B,A);howeverinmostOICreportsanimals receivedonlyonepreexposuretoeachofAandB[4,6–8,11,12,31]. Thisarrangementisproblematic,becauseitrendersinterpretation ofperformanceambiguous(cf.[7,12]).Forexample,considerthe casewhereAispre-exposedincontextx,andthenBincontext

y(Fig.1).Whenrecognitionistestedintheﬁrst,lessrecent con-text,x,thepresenceofxshouldresultinapreferenceforobjectB

becauseithasneverbeenpresentedinx.Butonthebasisof rel-ativerecencyonewouldanticipatetheopposite—apreferencefor objectA,becauseithasbeenencounteredearlierintheseries.As aresult,thetwoprocesseswouldcounteracteachotherwhenthe testisconductedintheﬁrstcontext.Incontrast,when recogni-tionistestedinthesecond,morerecentcontext,y,thecontext wouldleadtoapreferenceforobjectA,whichisthesameobject thatwouldbepreferredonthebasisofrelativerecency.Thushere

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incontexty.

Theseargumentsrestonthepredictionthatinthetask vari-antdescribedabove,OICperformanceissuperiorincontextythan incontextx.We wereunabletoevaluatethispredictiononthe basisof publishedwork[4,6–12,31];accordingly in thepresent articlewedescribetheﬁndings fromourown OICexperiments which,althoughperformedfordifferentscientiﬁcreasons,allow comparisonofperformanceincontextsxandyattest.

2. Experiment1

TwogroupsofratsweretrainedinthisversionoftheOICtask, receivingasinglepreexposureofobjectAincontextxfollowedbya singlepreexposureofobjectBincontexty.Therefollowedatestin whichanimalswerepresentedwithobjectsAandBsimultaneously, withanimalsinGroupxbeingtestedincontextx,and thosein Groupybeingtestedincontexty(Fig.1).Asoutlinedabove,we predictedthatforGroupx,RRandOICprocessesshouldcounteract eachother,resultinginaweakerdifferenceinexplorationbetween

AandBthaninGroupy,forwhomRRandOICshouldbothtendto producemoreexplorationofAthanofB.

2.1. Method

2.1.1. Subjects

Thesubjectswere12male,Listerhoodedrats(Rattus norvegi-cus; CharlesRivers,UK),housedinpairsinacryliccagesheldin anair-conditionedvivarium,whichwasilluminatedbetween0700 and 1900.The cages contained freshwoodchip bedding, and a largecardboardcylindertoprovide environmentalenrichment; waterandfoodwerefreelyavailable.Alltheratshadpreviously servedinaSkinner-boxexperiment,butwerenaivetothe appara-tusandstimulidescribedhere.Theexperimentwasconductedin tworeplications(n=8andn=4respectively;equalnumberswithin eachreplicationwereassigned toGroupsx andy). Atthestart ofthestudyratsinReplication1wereapproximately350g,and thoseinReplication2approximately500g.Twoofthefourrats inReplication2receivedsmallintra-peritonealinjectionsof phys-iologicalsalinebeforeeachofthetrialsdescribedbelow, which (basedonworkfromourlaboratory)wasknownnottoinﬂuence behaviour;one of theserats wasallocated toeach experimen-talgroup.Theproceduresreportedhereconstitutedpartoftwo, larger-scaleexperimentswhichincludedtreatmentgroupsthatare notrelevanttoourcurrentconcernsandwhosedataarethusnot consideredhere.

2.1.2. Apparatusandstimuli

Fourrectangulararenaswithwallsandfloorsofwhite translu-cent plastic (length×width×height: 60cm×40cm×45cm), locatedina quiet,brightly litroom,wereusedsimultaneously. Acamerawassuspended90.0cmabovethecentreofeacharena fromaframe.Eachcamera’sview(approximately45◦arc)included thecompletefloorbutonlythelowerpartofthefourwalls.Each camerawasflankedby two LED spotlights, 22cm apart, which producedafloor-levelilluminationof50lx;thesewereswitched on at the start of each phase and off when the phase ended. Any-maze software (version4.5; Stoelting,Wood Dale,IL)was usedtotrackeachrat’sheadlocationintwo-dimensionalspace intheplaneoftheapparatusfloor.Thesoftwarewascalibrated todetectablackregion-of-interest(i.e.,eachrat’shead)against awhitebackground.Thesoftwarecreatedtwo notionalcircular

objectzones of15-cmdiameter,which surroundedeachobject’s base;thesezones werelocatedalong thehorizontalmidline of theapparatus,andtheshortwalls weretangentstothezones;

thecreationofacumulativerecordofzoneentry.

Multiplecopiesofthreeobjectsservedasstimuli:(a)ablue, plasticbottle(20.0cminheightwithacircularbaseof7.0cm diam-eter);(b)amouldedplasticbottlecoveredwithblackandwhite penguins(20.5cm inheightwithmaximumbasedimensionsof 9.0cm×10.0cm);and(c),acylindrical,silveraluminiumvacuum ﬂask(19.5cminheightwithabaseof7.0cmdiameter).

Wallinsertsmadefrommediumdensityﬁbreboardlinedwith linoleumservedasthecontexts;thesecoveredthewholeofone oftheshorterwallsandhalfofbothlongerwalls(seephotographs inFig.1).Theseinsertswere45.0cmhighand,wheninsidethe box,gaveﬂoorspaceof42.0cm×32.0cm.Twodifferentpatterns wereused:Mb,amosaicof2.3cm2_blue_squares_whose_edges_were

45◦fromhorizontal(left-handsideofFig.1photograph),andDw, amosaicofwhite272-cm2 _squares_whose_edges_were₉₀◦_from

horizontal,withablack,16-cm2_square_superimposed_at_each_point

wherefourwhitesquaresmethorizontal(right-handsideofFig.1

photograph).

2.1.3. Procedure

2.1.3.1. Apparatuspre-exposure. Eachratwasexposedtothearena (withoutobjectsorinserts)forthreesessions,onesessionperday. Ineachsessiontheratwasplacedintheapparatusfacingthe mid-pointofthelongwallandallowedtoexplorefor10min.Thewall insertsandtheﬂooroftheapparatuswerecleanedwithdiluted alcoholaftereachrat’ssession.

2.1.3.2. Sampletrials. Eachratreceivedtwosample trialsof 10-minduration.Intheﬁrsttheratwasallowedtoexploretwocopies of anovel object(A)in one context:thetwo copies ofAwere placedatthecentresofthetwoobjectzones.Fiveminuteslater, ratsreceivedthesecondsamplephase,inwhichtheywereallowed toexploretwocopiesofadifferentnovelobject(B),positionedin asimilarmannerinthealternativecontext.Inbothreplications, halftheratsineachgrouphadcontextxasMbandcontextyas

Dw,andtheremainderthereverse;inReplication1halfofeachof thesetwosubgroupshadthebluebottleasAandthepenguinas

B,andtheremainderthereverse;inReplication2objectsAandB

werethepenguinandeitherasteelﬂask(n=3)orthebluebottle (n=1).

2.1.3.3. Test trials. The test trial occurred approximately 5min after the ﬁnal sample trial. Rats in Group x were tested in contextx(theﬁrst-sampledcontext)andratsinGroupyin con-text y. These trials were identical to the sample trials except that animals were presented simultaneously withone copy of

Aand one ofB.For approximately halftherats ineach group,

A was on the left and B on the right, and for the remainder thereverse.Datawererecordedfortheﬁrsttwominutesofthe test.

2.1.4. Datatreatment

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Fig.2. Meandiscriminationratiosfortheﬁrstandsecondminutesofthetestof Experiment1.Barsshowstandarderrorofthemean.

2.2. Results

ThetestdataaresummarizedinFig.2,andindicateastronger OICbiasinGroupythaninGroupx.Ananalysisofvariance(ANOVA) withgroupandminuteasfactorsconﬁrmedthisdescription, yield-ing a reliable main effect of grouponly, F(1, 10)=7.7, p<.020,

MSE=.073,2

p=.436,95%CI=[.01,.68];neitherthemaineffect

ofminutenortheinteractionwasreliable,smallestp>.100,F(1, 10)=3.2,MSE=.022.

2.3. Discussion

Our predictionwasthat performancewould bebetterwhen theanimalsweretestedincontextythancontext x,becausein theformer caseRRfacilitatesperformancewhileinthelatterit opposesit—andthatisexactlywhatweobserved.Incontrast, Nor-manandEacott[7]examinedperformanceseparatelyincontexts

xandy,butreportedthatthisfactorhadnostatisticalimpacton theirresults.Itisnotclearwhatcouldhaveproducedthis discrep-ancy,althoughNormanandEacott’s studydifferedina number ofwaysfromExperiment1.Forexample,intheirexperimentthe rats’explorationoftheobjectswaslimitedto30sineachsample phase.Thiscouldhavereducedthestrengthoftheobjects’memory tracesattest,thusreducingthecontributionofRRtotest perfor-mance.Mumbyetal.[6]alsoreportanon-signiﬁcantinﬂuenceof testingincontextsxandy,althoughtheirresultsnumerically par-alleledthoseofourExperiment1,showingsuperiorperformance incontextythanincontextx.

Thereare twootherpotentialexplanationsfor theresultsof Experiment1thatmust,however,beconsideredbeforeweaccept

thatRRmayoccurinOICtasks.First,thegeneralexperimental envi-ronmentmayhavebeenlessfamiliartotheratsduringthefirst sampletrialinxthanduringthesecondsamplephaseiny.Thus, throughprocessesseeninstandardobjectrecognition(e.g.,[1,2]), thesedifferencesincontextfamiliaritymighthaveresultedinmore explorationofxthanofy.Suchabiascouldinturninfluence explo-rationoftheobjects,resultinginlessexplorationofobjectAthan ofobjectB.Atendencyforthefirst-presentedobjecttobelesswell processed,ratherthanthefactthatitwaslessrecent,couldhave beenthereasonwhyperformancewasworseinGroupxthanin Groupy.Thesecondpossibilityisthatbothobjectswereprocessed equallywellinthetwosampletrials,butthatwhenanimalswere testedincontextx,becauseithadbeenexperiencedlongeragothan contexty,itmighthaveelicitedmorecompetingresponses,which maskedOICperformance.

Boththesealternativeexplanationsrelyonthesuggestionthat thetwocontextsdifferedintheirfamiliarity,eitherduring pre-exposureorattest. Sucha differenceisanintrinsic partof the procedureandsocannotbeentirelyeliminated,butitcanbe min-imized.ThiswasthepurposeofExperiment2(Fig.3).Inthisstudy allratswerepreexposedtobothcontextsbeforetheexperiment began,andtheexperimentwasconductedwithinsubjects,sothat allratsreceivedtrainingwithtwosetsofobjectsinthetwo con-texts,butweretestedwithonesetofobjectsincontextx,andwith theotherincontexty.Boththesefactorswouldincreasethe famil-iarityofbothcontextsandencouragefullhabituationofpotential competingexploratorybehaviour.Inaddition,theintervalbetween thesecondsampleandthetestphasewasextendedfrom5minto 2h,thusminimizingdifferencesintherelativerecencyofthetwo contexts.Finally,werecordedexplorationduringthetwosample trials,toexplicitlyevaluatethepossibilitythatthiscouldhave dif-ferentiallybiasedexplorationoftheobjectsduringthepreexposure phase.

3. Experiment2

3.1. Method

3.1.1. Subjects

FifteenListerHoodedmalerats(Harlan,Bicester,UK)wereused inthepresentstudy.Theyhadallreceivedshamoperationsofthe hippocampus;thustheywereanaesthetized,scalpincized,facial musclesretractedandaportionofthecranialboneabovethe hip-pocampusremovedwithanelectricdrill.A25-G,bevel-tipneedle wasloweredtoaseriesofsitesinthehippocampus,butno neu-rotoxinwaspassed.Thenthescalpwassutured,andtheywere allowedtorecoverfortwoweeksbeforethestartofbehavioural testing(fulldetailsofprocedurearedescribedin[18]),atwhich timetheyweighedapproximately400g.Theywerecagedinpairs exactlyasinExperiment1.Beforethestartofthisstudytheywere testedondifferentversionsoftheSORtask,butwerenaivewith respecttoboththecontextsandtheobjectsusedinthepresent study.

3.1.2. Apparatusandstimuli

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Fig.3.DesignofExperiment2.

high),andablackglassbottle(withabase9cmindiameterand 32cmhigh).Thezonesroundtheobjectsinthepresentexperiment were10cminradius,butotherwisearrangedasintheprevious experiment.

3.1.3. Procedure

3.1.3.1. Apparatuspre-exposure. Eachratwasexposedtothearena

withoutanyobjectsforfourdays,fortwosessionsperday.Inone ofthesetwo10-minsessions,thewallinsertsMbwereputinthe arena,whilefortheotherthewallinsertsDwwereused.Inallother respectsthesesessionswereidenticaltothoseofExperiment1.

AllratsreceivedtwocyclesofthefollowingOICprocedure,one oneachoftwoconsecutivedays.Eachcycleusedadifferentpairof objects,butthesamecontexts.

3.1.3.2. Sampleandtesttrials. Thesampletrialswereidenticalto thoseofExperiment1,exceptthateachsamplephaselastedonly 5min.Thetest trialstookplacetwo hoursaftertheend ofthe secondsamplephase,butwereotherwisesimilartothoseof Exper-iment1.FortheﬁrstOICsequence,8ratsweretestedincontextx

and7ratsincontexty;forthesecondallratsthatwereﬁrsttested incontextxwerenowtestedincontexty,andviceversa.Forthe ﬁrstOICsequencehalfofeachofthesegroups(ns=4and3)hadMb

asthecontextinsertinthefirstsamplephaseandDwinthesecond samplephase;thisarrangementwasreversedfortheremaining rats.Halfofeachofthesesubgroups(ns=2and1)hadtheduck inthefirstsamplephaseandthebottleinthesecond,andforthe remainderthereverse.Approximatelyhalfofeachofthese sub-groupsweretestedwithduckontheleftandbottleontheright, andfortheremainderthereverse.InthesecondOICsequencethe animalsthathadreceivedMbasthecontextinsertinthefirst sam-plephaseandDwinthesecondsamplephasecontinuedtodoso, asdidtheanimalsthathadexperiencedthereverse.The counter-balancingofthetwonewobjectsusedinthisphase,thecanand blackbottle,wasidenticaltothatinthefirstsequence.

3.2. Results

Oneaimofthisexperimentwastoexaminewhethertherewas lesstotalexplorationduringthefirstthanthesecondsampletrial; accordinglyexplorationduringthetwosampletrialsfromeachof thetwotestcycleswascomputed.Initialinspectionrevealedno influenceofthetestsequence(testinxbeforetestinyorviceversa), andsodatawerecollapsedacrossthisfactor.Themeanexploration timeforthefirstandsecondsampletrials(withSEMin parenthe-ses)were157.5s(1.3s)and151.2s(1.2s)forcycle1,and152.0s (1.6s)and160.0s(1.5s)forcycle2.AnANOVAwithcycle(firstand second)andsampletrial(firstandsecond)asfactorsrevealedno reliablemaineffects,Fs<1,orinteractionbetweenthosevariables,

F(1,14)=1.4,p>.263,MSE=562.337.Thustherewasnoevidence

Fig.4. Meandiscriminationratiosfortheﬁrstandsecondminutesofthetestof Experiment2.Barsshowstandarderrorofthemean.

forgreatercompetingresponsesintheﬁrstsampletrial,andthusno reasontosupposethatdifferentialexplorationofthetwocontexts hadasystematiceffectonexplorationofthetwoobjects.

The test data are summarized in Fig. 4. A test context (x

versusy)×minuteoftest(1stand2nd)repeated-measuresANOVA revealed a main effect of test context, F(1, 14)=4.6, p<.050,

MSE=.168,2

p=.250,95%CI=[.00,.93],againshowingOIC

perfor-mancetobebetterincontextythanincontextx.Themaineffect ofminuteoftestandthetestcontext×minuteoftestinteraction werenotreliablereliable,ps>.40.

3.3. Discussion

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evidenceofanydifferenceinexplorationinthetwosamplephases ineithercycleoftesting,makingitdifﬁculttoarguethatobjectA

waspreferrednotbecauseitwaslessrecentperse,butbecauseit hadbeenlesseffectivelyexploredthanobjectB,asaresultof com-petingbehaviourprovokedbytherelativelynovelenvironmenton theﬁrstsampletrial.Moreover,theincreasedexperiencewiththe twocontexts,andtheincreaseddelaybetweenthesecond sam-plephaseandthetest,willhaveminimizedthepossibilitythat contextxselectivelyinterferedwithperformanceontestsimply becauseithadbeenexperiencedlessrecently.Thustheresultsof thesetwoexperimentsareconsistentwithourpredictionthatRR caninﬂuenceperformanceinOICtasks.

4. Generaldiscussion

Thepresentresultsdemonstratethatinthemostcommonly usedversionoftheOICtask(e.g.,[4,6–12,31]),inwhichanimals receiveonlyonesampletrialwitheachofthetwoobjects, per-formance wasreliably betterwhen the animalswere tested in themost recent context.We have interpretedthis asevidence thatperformancedoesnotdependsolelyonthecontextinwhich thetestisconducted,butalsoontheRRofthetwotestobjects

[16–18,20]—The suggestionis that, when animalsare tested in theﬁrstofthetwocontexts,RRopposestheeffectofthecontext, whereaswhentheyaretestedintheseconditexaggeratesit.This versionofthetaskdoesnot,therefore,provideapuremeasureof theabilityofanimalstoencodethecontextinwhichaparticular objectwaspresented,ortheeffectofthisonsubsequentmemory performance.

4.1. Empiricalimplications

WeofferfourrecommendationstominimizetheimpactofRR and/ortoexaminethesizeofRRinOICexperiments:

4.1.1. Lengthofretentioninterval

Accordingtotheanalysiswehaveoffered[18,20,28–30], exten-sionoftheintervalbetweenthefinalsampletrialandtesting(the retentioninterval)mayallowthememorytracesfromthesample trialstodecaytotheirinactivestates(i.e.eliminatingthesourceof RR).Withsuchanarrangement,onlytheintended,retrieval-based sourceoftest performancewilloccurontest (i.e.OIClearning). Thepointatwhichdecayiscompletecouldbedeterminedby sys-tematicvariationoftheretentionintervalinRRexperiments:In particular,thepointatwhichtheretentionintervaleliminatesRR discriminationwillcorrespondtothepointatwhichthesample memorieshavebecomeinactive.Theeffectiveretentioninterval canthenbeusedtoaccuratelyassessOIClearning.Intheabsence ofsuchinformationitwouldseemsufficienttouse24-hretention intervals[9,10],whicharelikelytobesufficientlylongtoallow completememorydecay.

4.1.2. Numberofpreexposuretrials

SomemodiﬁcationstothedesignoftheOICexperimentcanbe usedtoreduceRR.AmorecomplexversionoftheOICprocedure, originallyemployedbyDixandAggleton[5],islesssusceptibleto thepotentialinﬂuenceofRR,becauseherethetwoobjectsare pre-exposedtwicein adouble alternatingsequence(i.e.,xA,yB,yB,

xAforhalfoftheratsandyB,xA,xA,yBfortheremainder).This treatmentensuresthatthepresentationorderofthetwoobjects ismatched(i.e.,objectAbeingpre-exposedinpositions1and4, andBinpositions2and3,each withanidenticalmidpoint).Of coursewhetherthismatchingintermsofpresentationordercan betranslateddirectlyintomatchingofmemorytracesis question-able,aswecannotsafelyassumethatthememorytracefroman

objectexposedontheﬁrstandfourthtrialsisequivalenttothat pre-sentedonthesecondandthird.Suchinequalitymaybetheresult ofanonlineardecayrate—acharacteristicofmemoryperformance (e.g.,[32–34])—orfromdifferentialinterferencestemming from differencesinthenumberofinterveningpreexposuretrials[27]. Thuseventheuseofdouble-alternatingsequencesdoesnotentirely avoidpotentialeffectsofRR.Itisalsonotablethatsomeresearchers maywishtouseapairofsinglesampletrialstomodelepisodic memoryprocesses[16,31,35],althoughsomehavequestionedthe logicofmappingsingle-triallearningontoepisodicmemory[36].

4.1.3. Arrangementofpreexposuretrials

AthirdvariantoftheOICprocedureavoidsthepotential inﬂu-enceofRRbycombiningthetwosamplepairingsintoasingletrial. Forexample,Good,Barnes,Staal,McGregor,andHoney[16]gave ratsasinglesampletrialinwhichfourobjectswerelocatedinthe fourcornersoftheexperimentalarena.Inthesubsequenttest,the locationsoftwooftheobjectsthatwerelocatedinopposite cor-nerswereswitched.Wemayassumethattheswitchedobjectsmay haveenteredintoassociationwiththetwoadjacent,un-switched objectsduringthesinglesampletrialorwithextra-arenacuesin thelaboratory.Theseassociationscanbethoughtofasanaloguesof thex/ycontextassociationsinotherOICprocedures;thus compar-isonofexplorationoftheswitchedandunswitchedobjectsgivesa measureofOIClearning.

4.1.4. Analysisofsubgroups’data

Evenwhenusedwiththerecommendationsabove,ourresults demonstratetheimportanceofanalysisofdatafromthe counter-balancedsubgroupsthatreceivetestingincontextxorcontexty. Theoutcomeofthisanalysismaybethatthereisnoevidenceofthe involvementofRRinOIC(cf.[6,7]),inwhichcaseresultssuchas theeffectsofneuralmanipulationsmaybeinterpreted straightfor-wardly.However,whenRRisdetectedduringOIC,effectsofneural manipulationsareambiguous—Theirsourcescouldbe,e.g.,adeﬁcit inRR,OIC,orboth.Forthesamereasonsitmayalsobe interest-ingforresearcherstoreportsuchnewanalysesoftheirpreviously publishedwork.

4.2. Theoreticalinterpretation

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proportionofitselementsarestilllikely toberesidingintheir secondarystatesofactivity.Butmoreremotelypresentedobjects, whoseelementshaveentirelydecayedtoinactivity,willbeable toelicitstrongerapproachrespondingbecausetheirelementscan passdirectlyintotheirprimaryactivitystate.Theseassumptions provideanexplanationofperformance inanRRexperiment:at testagreaterproportionofthelessrecentobject’selementswill havebecomeinactive,allowingthemtoentertheprimary acti-vationstatewhentheobjectispresentedattest[18,28].Similar logiccanofferanexplanationofperformanceinthesimpleSOR task,asthenovelobject’selementsareallabletoenterthe pri-maryactivation state, whereas those of thefamiliar object are not.

Asecondcritical assumptionofSOP isthat whentwo items are associated, presentation of one will place elements of the otherdirectlyintothesecondaryactivation state.Thisprovides analternativeanalysisofSOR,bysupposingthatapparatuscues enterintoanexcitatoryassociationwiththeobjectduringthe pre-exposurephase.Attest,theapparatuscuesplacetheelementsof thepre-exposedobjectintothesecondaryactivationstate, reduc-ingthedegreetowhichitisexplored.Incontrastthenovelobject, beingun-associated withtheapparatuscues, isnotexpectedin theapparatus,soitselementsareinactiveandcanenterthe pri-maryactivationstatewhenitispresented;thusnormallevelsof explorationaremaintained[18,20,28–30].OICperformancecanbe explainedinasimilarmanner;althoughbothobjectsare associ-atedwiththeirrespectivecontexts,attestonlytheelementsof theobjectin itspreexposure contextwill beassociatively acti-vated.Thus theelementsof thealternativeobjectwillbemore abletoentertheprimaryactivationstateandelicittheexploration response.

Thus SOP proposesthat RRdepends ondifferential decayof thestimuluselementsofthetwoobjects,whileOICstemsfrom differencesintheirassociativeactivation—andthereisnothingin themodelwhichwouldprecludebothprocessesoperatinginthe same task. Thus a model of this type should easily beable to accommodatetheresultsreportedhere—asuggestionwhichwe haveconﬁrmedinunpublishedcomputersimulations.Moreover, althoughitcanexplainperformanceonthesetasksaswellasother theoriesofobjectrecognition,itcanalsoexplainagreatvariety ofassociativelearningeffects.Thisbreadth,wewouldargue,gives thismodelanedgeoverthosewhoseexplanatorypowerislimited toobjectrecognitionmemory.

5. Conclusion

Theresultsof thepresent experiments demonstratethat, in themostwidelyusedvariantoftheobject-in-placetask,relative recencycancontributetoperformance.Thispossibilitypotentially complicatesinterpretationoftheresultsfromexperimentsusing thisprocedure,andwesuggestanumberofrecommendationsto minimize,oratleastmonitor,theeffectofRRonOICperformance. Ourresultsarealsoconsistentwithanassociativeaccountof recog-nitionmemory,whichexplainsperformanceinSOR,RRandOIC tasksintermsofthesameunderlyingmechanism.

Acknowledgements

Work reported here was funded by BBSRC grants to CB (BB/E019196)andJR(BB/C006283/1).Workdescribedherewasin partialfulﬁlmentofSKET’sPhD,whichwasfundedbytheSchool ofPsychologyandInternationalOfﬁce,UniversityofNottingham.

inourreport.

ProcedureswereauthorizedunderUKlaw,Animals(Scientiﬁc Procedures)Act(1986).

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