Imagining Other People's Experiences in a Person with Impaired Episodic Memory: The Role of Personal Familiarity.

1.3 MB·English

by  Rabin, Jennifer S.

ORIGINALRESEARCHARTICLE
published:24January2013
doi:10.3389/fpsyg.2012.00588
Imagining other people’s experiences in a person with
impaired episodic memory: the role of personal familiarity
JenniferS.Rabin1*,NicoleCarson1,AsafGilboa2,3,4,DonaldT.Stuss2,3,5,6,7 andR.ShaynaRosenbaum1,2
1DepartmentofPsychology,YorkUniversity,Toronto,ON,Canada
2RotmanResearchInstitute,BaycrestHospital,Toronto,ON,Canada
3DepartmentofPsychology,UniversityofToronto,Toronto,ON,Canada
4TheHeartandStrokeFoundation,CentreforStrokeRecovery,Toronto,ON,Canada
5OntarioBrainInstitute,Toronto,ON,Canada
6DivisionofNeurology,DepartmentofMedicine,UniversityofToronto,Toronto,ON,Canada
7RehabilitationSciences,UniversityofToronto,Toronto,ON,Canada
Editedby: Difficultiesrememberingone’sownexperiencesviaepisodicmemorymayaffecttheability
R.NathanSpreng,CornellUniversity, toimagineotherpeople’sexperiencesduringtheoryofmind(ToM).Previousworkshows
USA
that the same set of brain regions recruited during tests of episodic memory and future
Reviewedby:
imaginingarealsoengagedduringstandardlaboratorytestsofToM.However,hippocampal
SimoneG.Shamay-Tsoory,University
ofHaifa,Israel amnesicpatientswhoshowdeficitsinpastandfuturethinking,showintactperformance
JanelleBeadle,UniversityofIowa, onToMtests,whichinvolveunknownpeopleorfictionalcharacters.Herewepresentdata
USA fromadevelopmentalamnesicperson(H.C.)andagroupofdemographicallymatchedcon-
*Correspondence: trols,whoweretestedonanaturalistictestofToMthatinvolveddescribingotherpeople’s
JenniferS.Rabin,Departmentof
experiences in response to photos of personally familiar others (“pToM” condition) and
Psychology,YorkUniversity,4700
KeeleStreet,Toronto,ON,Canada unfamiliar others (“ToM” condition).We also included a condition that involved recollect-
M3J1P3. ing past experiences in response to personal photos (“EM” condition). Narratives were
e-mail:[email protected] scoredusinganadaptedAutobiographicalInterviewscoringprocedure.Duetothevisually
rich stimuli, internal details were further classified as either descriptive (i.e., details that
describethevisualcontentofthephoto)orelaborative(i.e.,detailsthatgobeyondwhat
is visually depicted in the photo). Relative to controls, H.C. generated significantly fewer
elaborativedetailsinresponsetothepToMandEMphotosandanequivalentnumberof
elaborativedetailsinresponsetotheToMphotos.Thesedataconvergewithpreviousneu-
roimaging results showing that the brain regions underlying pToM and episodic memory
overlaptoagreaterextentthanthosesupportingToM.Takentogether,theseresultssug-
gestthatdetailedepisodicrepresentationssupportedbythehippocampusmaybepivotal
forimaginingtheexperiencesofpersonallyfamiliar,butnotunfamiliar,others.
Keywords:episodicmemory,theoryofmind,hippocampus,amnesia,socialcognition
INTRODUCTION toimagineone’sownpersonalfuture.Amnesicindividualswith
Amnesia following damage to the hippocampus has been char- hippocampaldamagewhoareunabletorecollectpasteventsalso
acterized by impaired episodic memory for personally experi- have difficulty imagining themselves in future events (Tulving,
encedevents.However,thereisgrowingevidencethatother,non- 1985;Kleinetal.,2002;Rosenbaumetal.,2005;Andelmanetal.,
mnemonic processes may be compromised in amnesia as well. 2010). Consistent with this finding, neuroimaging studies have
Thesefindingshaveledresearcherstosuggestabroaderrolefor revealed that both abilities recruit a similar set of brain regions
thehippocampusandepisodicmemorythatgoesbeyondrecall- thatincludethehippocampusandadjacentmedialtemporallobe
ingpastpersonalexperiences.Muchofthisworkhasfocusedon (MTL)regionsaswellasmedialfrontal,medialparietal,andlateral
theideathatepisodicmemoryisnecessaryforimaginingpossible temporal cortex (Okuda et al.,2003;Addis et al.,2007;Szpunar
future scenarios (Tulving,1985; Klein et al.,2002; Okuda et al., etal.,2007).Someofthesestudieshaveincludedacontrolcondi-
2003; Rosenbaum et al.,2005;Addis et al.,2007; Szpunar et al., tion in which participants are asked to imagine the experiences
2007;Andelmanetal.,2010),whereasmuchlessattentionhasbeen of an “average” person or a famous person, which appears to
paidtotherolethatepisodicmemoryplaysinsocialbehavior.In engage regions within the MTL as well,albeit to a lesser extent
thecurrentstudy,weexaminedif,andunderwhatconditions,the (Szpunaretal.,2007;seealsoGilboaetal.,2004).However,itmay
abilitytorememberandimagineone’sownexperiencesservesa be the case that episodic memory and associated MTL function
socialfunctioninfacilitatingtheabilitytoimagineotherpeople’s play an important role in imagining other people’s experiences,
experiences. assuggestedbyqualitativereviewsandmeta-analysesoftheneu-
Animpressivebodyofresearchhasshownthatepisodicmem- roimagingliterature.Thesestudiesshowthatthesamesetofbrain
ory,supportedbythehippocampus,iscloselyrelatedtotheability regions activated during tests of episodic memory and future
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Rabinetal. Episodicmemoryandimaginingothers’experiences
imagining are also engaged during standard tests of theory of similartotheselfandwhentheeventhadoccurredinthepartici-
mind (ToM; Buckner and Carroll,2007; Hassabis and Maguire, pant’sownlife.Takentogether,thesestudiessuggestthatepisodic
2007;Sprengetal.,2009). memorymayserveasocialroleinimaginingotherpeople’sexpe-
In addition to an overlapping set of brain regions, episodic riences,but only when intimacy or closeness exists between the
memory, future imagining, and ToM emerge close in time in participantandtheperceivedother.
ontogenetic development (Perner and Ruffman, 1995; Atance Inthecurrentstudy,wetesttheideathatepisodicmemoryis
and O’Neil, 2001; Perner et al., 2007) and tend to be impaired necessaryforimaginingeventsfromtheperspectiveofpersonally
in patients with schizophrenia (Corcoran and Frith, 2003; knownothers.Onewaytoaddressthisquestionistoassesswhether
D’Argembeau et al., 2008) and high functioning autism and apersonwithhippocampalamnesiaandimpairedepisodicmem-
Asperger’ssyndrome(Adleretal.,2010;LindandBowler,2010). oryisabletoimagineeventsexperiencedbywell-knownothers,
Thesefindingslendsupporttoaninfluentialtheoreticalperspec- includingreconstructingothers’thoughtsandfeelings.Here,we
tivethatindividualsdrawonpastexperiencesviaepisodicmemory testH.C.,auniqueyoungwomanwithnormalintellectualfunc-
tosimulatefuturepersonalexperiencesandtoimagineotherpeo- tiondespiteimpaireddevelopmentofherepisodicmemorydueto
ple’sexperiencesduringToM(Gordon,1986;Goldman,1992;Cor- selectivehippocampaldamage1weekafterbirth(Vargha-Khadem
coran,2000,2001;GallagherandFrith,2003;BucknerandCarroll, etal.,2003;Rosenbaumetal.,2011;seealsoKwanetal.,2010;Hur-
2007; Schacter and Addis, 2007; Spreng and Mar, 2012). How- leyetal.,2011).Importantly,aswasthecasefortheadult-onset
ever,work with hippocampal amnesic patients shows preserved hippocampal amnesic cases described above, we recently found
performanceonstandardtestsofToMdespiteimpairedepisodic that H.C.’s performance on a wide range of standard ToM tests
memory and future imagining (Rosenbaum et al., 2007; Rabin was indistinguishable from that of controls (Rabin et al.,2012).
etal.,2012).StandardToMtestsincludedinthesestudiesranged WebelievethatherpreservedToMperformanceisduetoreliance
frompredictingacharacter’sfalsebelief (Stoneetal.,1998)and onhersemanticmemoryandgeneralknowledgeabilities,which
identifyingafauxpas(Stoneetal.,1998)basedonnarratives,to remainrelativelyintact(Rabinetal.,2012).Inthecurrentstudywe
inferringothers’thoughtsandemotionsbasedonviewingtheeye employedanaturalistictestof ToMthatinvolveddescribingthe
regionoffaces(Baron-Cohenetal.,2001).Theamnesicpatients’ experiences of other people in response to photos of personally
successful performance on these tests may have been achieved known others (i.e., relatives and close friends; “pToM” condi-
via semantic memory, which remains relatively intact in these tion)andunknownothers(“ToM”condition)engaginginspecific
patients(Rosenbaumetal.,2007).Thismightincluderelianceon events.Wealsoincludedaconditionthatinvolvedrecollectingpast
social knowledge of the average person’s thoughts,feelings,and experiencesinresponsetopersonalphotos(“EM”condition).This
intentionsindifferentcircumstances(Lieberman,2012). naturalistic task was selected because it is less constrained than
More recent neuroimaging studies have directly compared moststandardtestsofToMandthereforebettercapturesToMas
episodicmemorywithToMinthesameindividualsusingmore itoccursineverydaylife.FindingsofimpairedpToMthatparal-
naturalisticstimuli(Rabinetal.,2010;SprengandGrady,2010;St. lelH.C.’sepisodicmemorydeficitwouldsuggestthatpToMrelies
Jacquesetal.,2011;seealsoGilboaetal.,2004;Szpunaretal.,2007). on episodic memory or that a common process mediates both
Thesestudiesrevealedthatrelativetorecallingpastepisodes,imag- abilities. Alternatively, it may be the case that intact aspects of
iningtheexperiencesof otherpeopleelicitedlessactivitywithin H.C.’s semantic memory are sufficient to support mental state
MTL and midline regions. However,the“other”targets in these inferences involving pToM and ToM,and therefore H.C. would
studieswerenotintimatelyknownbyparticipants(i.e.,strangers showintactperformanceonbothtasks,similartoherperformance
or public figures). It is possible that when the target person is onstandardToMtests.
personally known,shared past experiences can influence partic-
ipants’current social processing. Indeed, knowing someone for MATERIALSANDMETHODS
a long period of time and observing that person’s behavior in PARTICIPANTS
different situations provides a rich source of information from H.C.isaright-handedwomanwhowas20yearsoldatthetime
whichonecandrawwhenimagininghis/hermentalstatesinspe- of testing. A second testing session was performed when H.C.
cificsituations.Consistentwiththisidea,RabinandRosenbaum was 23years old for reliability purposes. She was born prema-
(2012) recently showed that imagining the experiences of per- turelyandsufferedhypoxicdamage,whichledtoreducedbilateral
sonally familiar versus unfamiliar others preferentially engaged hippocampal volume by approximately 50% relative to healthy
regionsknowntosupportepisodicmemory,suggestingastrategy controls (Vargha-Khadem et al., 2003; Hurley et al., 2011; see
ofrelyingonpastpersonalexperienceswhenthetargetpersonis Rosenbaumetal.,2011foradetailedneuropsychologicalprofile).
personallyknown.Inanotherstudy,Krienenetal.(2010)focused H.C.’scompromisedbilateralhippocampaldevelopmentappears
exclusivelyonmidlinefrontalregionsandfoundgreateranterior tohaveprecludednormaldevelopmentofherepisodicmemory.
medialprefrontalcortexandrostralanteriorcingulatecortexactiv- Her impairment affects her personal and public event memory
ityforjudgmentsrelatingtoparticipants’friendsversusstrangers. more than her personal and general semantic memory (Rosen-
Infact,participantsinthatstudyindicatedthattheyreliedonaspe- baumetal.,2011),whichisconsistentwithotherdevelopmental
cificmemoryoranecdotesignificantlymoreoftenforjudgments amnesic cases (Gadian et al.,2000). H.C. successfully graduated
relatingtofriendsthanstrangers.Perryetal.(2011)showedthat fromamainstreamhighschoolandcompleted1yearoftechnical
hippocampalactivityduringjudgmentsofothers’emotionalstates college.At the time of the first testing session,she was enrolled
was specific to conditions in which the protagonist was deemed inapost-secondaryculinaryprogrambutwithdrewafter1year.
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Rabinetal. Episodicmemoryandimaginingothers’experiences
H.C.hasformedanormalnumberofcloserelationships(David- inasmuchdetailaspossible.Theyweretoldtofocusonwhatthey
sonetal.,2012,thisissue)andwasengagedtobemarriedatthe werethinkingandfeelingatthetime.
secondtimeoftesting. Following the presentation of each photo, participants rated
H.C.’s performance on all measures was compared with that the events they imagined/recollected on a number of dimen-
of 18 right-handed,healthy women with no reported history of sions. Three ratings scales were presented after each photo. The
neurological or psychiatric illness (mean age=19.4, SD=1.3; firstratingscaledifferedforthepToM/ToMandEMevents.The
meaneducation=13.3,SD=1.1).Allparticipantsgaveinformed pToMandToMeventswereratedforlikenesstoanactualmem-
written consent in accordance with the ethics review boards ory (1=exactly like a memory ... 4=nothing like a memory),
atYork University and Baycrest. Participants received monetary whereas the EM events were rated on the extent to which the
compensationfortheirtime. events were recollected (1=don’t know event;2=familiar with
event;3=rememberevent;Gardineretal.,1998;Tulving,1985).
STIMULI Participantswereinstructedtoselect“remember”iftheeventwas
We employed a novel, naturalistic test of ToM that involved specific to a time and place and they could re-experience it, to
describing others’ thoughts and feelings in response to photos select“familiarwithevent”iftheeventwasfamiliartothem,but
of personally familiar others (“pToM”condition) and unfamil- theycouldnotrecallanyspecificcontextualorotherexperiential
iar others (“ToM” condition) engaging in specific events. We detailsassociatedwiththeevent,andtoselect“don’tknowevent”
also included a condition that involved recollecting past experi- iftheywereunabletorecallanyaspectoftheevent.Thenexttwo
encesinresponsetopersonalphotos(“EM”condition;Rabinand ratingsscaleswereemployedforallconditions.Onescaleassessed
Rosenbaum,2012). theamountof detailgeneratedforeachevent(1=notvivid...
ThepToMconditioninvolvingpersonallyknownotherscon- 4=veryvivid)andtheotherscaleassessedthespatialcoherenceof
sistedof 15photosdepictingspecificeventsthathadbeenexpe- eachevent(contiguousnessofthespatialcontext:1=fragmented
rienced by family members and close friends but not by the scenes...4=continuousscene;Hassabisetal.,2007;notreported
participant him/herself. The ToM condition involving unfamil- inthecurrentstudy).
iarothersconsistedof 15photosdepictingstrangersengagedin Prior to the scan, a short training session was provided to
specificevents.TheEMconditionconsistedof15personalfamily ensure that participants fully understood the task instructions.
photos of events that took place within the past 1–5years. H.C. The photos used in the training session were not used during
and13ofthe18controlparticipantsappearedineachEMphoto thescan.
tohelpverifythattheparticipantpersonallyexperiencedtheevent. Immediately following the scan,participants took part in an
Analysesconfirmedthatthepresenceorabsenceofthecontrolpar- interview in which they viewed the same photos that had been
ticipantsintheEMphotosdidnotaffectthebehavioralresults(i.e., presentedinthescanner.Participantswereaskedtothinkbackto
averagenumberof internaldetailsdidnotdiffer,t(16)=−0.47, theeventstheygeneratedinthescannerandtorateeacheventon
p=0.64). The pToM and EM photos were collected by a rela- thesamethreescalesthatwerepresentedinthescanner.Thepho-
tiveorclosefriendof eachparticipant,whereastheToMphotos toswiththehighestvividnessratings(approximatelytwo-thirds
were collected by the experimenter. Themes were similar across of all photos) were selected for a semi-structured interview in
the three conditions (e.g., birthday party, picnic, vacation) and which participants described the events as they had been imag-
includedbothindoorandoutdoorscenes.Allphotoswereresized ined/recollectedinthescanner.1Highvividnessratingsweretaken
andconvertedtograyscale. tosuggestthatparticipantswereindeedimaginingorrecollecting
theevents.Therewasnotimelimitforparticipantstodescribethe
TASK events, and participants continued with their descriptions until
H.C.andthecontrolparticipantswerescannedwithfMRIwhile they came to a natural ending point. The examiner then pro-
performingthefamilyphotostask(fMRIdatanotreportedhere). videdasingle,standardizedprobetoelicitadditionaldetails(e.g.,
Stimuli were presented in blocks and each block contained five “Canyoutellmeanythingelse?”).Theeventswererecordedand
photosfromoneofthethreeconditions.Therewerethreeblocks transcribedforscoring.
foreachcondition(foratotalofnineblocks)andthesewerepre- Controlparticipantsweretestedonthefamilyphotosparadigm
sented in pseudorandom order.At the beginning of each block, once whereas H.C. was tested on the paradigm on two separate
participantsviewedasetofinstructionsthatcorrespondedtoone occasions for reliability purposes. However, the EM events that
of the three conditions (i.e., pToM, ToM, or EM). Each photo were included during H.C.’s first testing session were excluded
waspresentedfor20sandwasfollowedbythreeratingscales(see because we subsequently learned that she frequently views and
below). rehearsestheeventsdepictedinthesephotos.
InthepToMandToMconditions,participantswerepresented
withphotosofotherpeopleandaskedtogenerateanoveleventfor SCORING
eachphotowhilefocusingonwhatonepersoninthephotomight NarrativeswerescoredusinganadaptedAutobiographicalInter-
have been thinking and feeling at the time. In order to distin- view scoring procedure described by Levine et al. (2002). The
guishimaginingfromremembering,participantswerespecifically
instructednottodrawonpastexperienceswhengeneratingthese
1Duringsession2,H.C.wasinterviewedonallofthephotospresentedduringthe
events.IntheEMcondition,participantswerepresentedwiththeir
scanaswellaseightadditionalEMevents,whichwerenotpresentedinthescanner,
ownphotosandaskedtorecollecttheeventdepictedineachphoto inordertoincreasepower.
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Rabinetal. Episodicmemoryandimaginingothers’experiences
pToM, ToM, and EM events were first segmented into distinct 7pToMeventsand9ToMeventstotheanalyses.Insession2,H.C.
details,whichwereclassifiedasinternal(includingevent-specific, contributed15pToMevents,12ToMevents,and18EMeventsto
temporal, perceptual, spatial, and thought/emotion details) or theanalyses.
external (i.e., semantic facts that were irrelevant to the central
event,repetitions,and metacognitive statements). Given the use PHENOMENOLOGYOFTHEpToM,ToM,ANDEMEVENTS
ofvisuallyrichphotosascues,wewantedtoensurethatpartici- We entered participants’ post-scan ratings into the analyses (as
pants’performancewasnotinflatedduetomerelydescribingthe opposedtothewithin-scannerratings)asthesewerebelievedto
detailsdepictedinthephotos.Therefore,internaldetailswerefur- better correspond with the events participants described during
ther classified as either descriptive (i.e.,details that describe the thepost-scaninterview.Table2presentsparticipants’phenome-
visual content of the photo) or elaborative (i.e., details that go nologicalratingsofthepToM,ToM,andEMevents.Intermsof
beyond what is visually depicted in the photo; see Table 1 for vividness,H.C.ratedthepToMeventsinsession1aslessvividthan
scoringcriteria). controls,t(17)=−2.68,p=0.02;therewasnodifferenceforthe
Scoring of the narratives was conducted by a trained rater pToMeventsinsession2,t(17)=−0.73,p=0.48.Withrespectto
who achieved high interrater reliability on the Autobiographi- theToMevents,vividnessdidnotdifferbetweenH.C.andcontrols
calInterviewusingastandardsetofpreviouslyscoredmemories forsession1,t(17)=−0.97,p=0.34,orsession2,t(17)=−1.46,
(see Levine et al., 2002). Interrater reliability was also calcu- p=0.16.FortheEMevents,H.C.’sratingsweresignificantlyless
latedfortheelaborativeanddescriptivedetailsbasedoncriteria vividthanthatofcontrols,t(17)=−3.89,p=0.0006.Intermsof
developed by JSR. Intraclass correlation analyses indicated high theratingsassessinglikenesstoanactualmemory,nosignificant
agreementamongscorersforpToM(Cronbach’sα=0.994),ToM differencesemergedbetweenH.C.andcontrolsforthepToMand
(Cronbach’sα=0.992),andEMevents(Cronbach’sα=0.994). ToMeventsinsession1orsession2[pToMsession1andsession2,
Datawereanalyzedusingamodifiedt-testprocedure,which t(17)=−1.56,p=0.14,andt(17)=−0.38,p=0.70,respectively,
comparestestscoresofasinglepatienttothatofasmallcontrol and ToM session 1 and session 2, t(17)=−0.58, p=0.57, and
sample(CrawfordandHowell,1998).Two-tailedt-testswereused t(17)=−0.58,p=0.57,respectively].Finally,asexpected,H.C.’s
tocompareH.C.’sperformancewiththatofcontrolsonthepToM ratingsrelatingtotherecollectionofEMeventsweresignificantly
andToMconditions,whereasaone-tailedt-testwasusedforthe lowerthanthatofcontrols,t(17)=−9.73,p<0.00001.
EMconditiongivenapriorihypothesesregardingH.C.’sepisodic
memoryperformance. ADAPTEDAUTOBIOGRAPHICALINTERVIEW
Given the use of visually rich photos as cues, we were most
RESULTS interested in the elaborative details that participants generated.
Asmentionedabove,H.C.wastestedontwoseparateoccasions. We analyzed the data in two ways. First,we compared the aver-
Forcompleteness,wereportthedataseparatelyforthetwotesting age number of elaborative details H.C. and controls produced
sessions. Each control participant contributed an average of 8.9 in response to each pToM,ToM,and EM event. These absolute
pToMevents(SD=0.72),9.1ToMevents(SD=0.9),and9.3EM numbers, however, are confounded by participants’ total verbal
events(SD=0.49)totheanalyses.Insession1,H.C.contributed output.Toovercomethisissue,wealsocalculatedtheproportion
Table1|Classificationofdescriptiveversuselaborativedetails.
Typeofdetail Descriptivedetails Elaborativedetails
Action Anydetailreferringtoanactionthatisdepictedinthephoto Anydetaildescribinganactionthatisnotobviousfromthe
(e.g.,sitting,walking,standing,posingforthephoto) photo
Character Anydetailexplainingwhothepeopleareinthephoto(onlyfor Anydetaildescribingwhothepeopleareoranydetailthat
thepToMandEMconditions) referstotherelationship(s)betweenthepeopledepictedinthe
photo(onlyfortheToMcondition)
Temporal N/A Anydetailreferringtoaspecifictimeperiod(e.g.,year,season,
month,date,dayofweek)
Perceptual Perceptualdetailsthataredepictedinthephoto(e.g.,big Perceptualdetailsthatarenotvisibleinthephoto
crowdofpeople,candleseverywhere).
Describingornaminganobject,monumentorstatuethatis
depictedinthephoto(e.g.,StatueofLiberty)
Emotion/thought Anydetaildescribingafacialexpression(e.g.,smiling, Anydetaildescribinganemotionormentalstate(e.g.,happy,
frowning) sad,tired)
Spatial/Place Anydetaildescribingalocation(e.g.,country,city,street, Anydetaildescribingalocation(e.g.,country,city,street,
locationwithinaroom)thatcanbeinferredfrominformation locationwithinaroom)thatisnotapparentfrominformation
presentedinthephoto(e.g.,sign) depictedinthephoto
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Table2|PhenomenologicalqualitiesofthegeneratedpToM,ToM,and knownothers,whichresembleshercompromisedabilitytorecall
EMevents. pastexperiencesviaepisodicmemory.Theseimpairmentsstand
incontrasttoherpreservedabilitytoimaginetheexperiencesof
pToM ToM EM
unknown others. This pattern of results held whether we ana-
lyzed the average number of elaborative details (i.e.,details that
Vividness
go beyond what is visually depicted in the photo) or the pro-
H.C.session1 2.1* 2.7 –
portionofelaborative-to-total-internaldetailsinordertocontrol
H.C.session2 2.9 2.5 2.8*
forverbaloutput.Theseresultsbolsterthefindingthatdifferent
Controls 3.2(0.4) 3.1(0.4) 3.6(0.2)
neural and cognitive mechanisms support thinking about per-
Remember/know
sonallyknownversusunknownothersandthattheformermay
H.C.session1 – –
dependonprocessesmediatedbythehippocampusandepisodic
H.C.session2 – – 2.6*
memory.
Controls – – 3.0(0.04)
The idea that individuals rely on past personal experiences
SimilartoaMemory
to infer and simulate another’s mental state has been suggested
H.C.session1 2.7 3.3 –
by philosophers and cognitive neuroscientists alike (Corcoran,
H.C.session2 3.3 3.3 –
2000,2001;GallagherandFrith,2003;BucknerandCarroll,2007;
Controls 3.5(0.5) 3.6(0.5) –
SprengandMar,2012).However,thecurrentfindingsindicatethat
Standarddeviationsaregiveninparentheses;pToM,personaltheoryofmind; reliance on past personal experiences may be pivotal only when
ToM,theoryofmind;EM,episodicmemory;*p<0.05. imagining the experiences of personally known others. Indeed,
knowing an individual for a long period of time and observ-
ofelaborative-to-totalinternaldetails,whichprovidesanindexof ing that person’s behavior in different situations provides a rich
theweightgiventodescriptiveversuselaborativedetails. source of information from which one can draw when imagin-
The mean number of elaborative details produced by par- ing his/her mental states in various situations. Consistent with
ticipants in response to each pToM, ToM, and EM event is thisinterpretation,Krienenetal.(2010)showedthatparticipants
presented in Figure 12. In response to the pToM events, H.C. reported that they relied on a specific memory or anecdote sig-
producedsignificantlyfewerelaborativedetailsthancontrolsdur- nificantlymoreoftenwhenmakingjudgmentsrelatingtofriends
ing session 1, t(17)=−3.1, p=0.007, and there was a trend relativetostrangers.Inanotherstudy,Ciaramellietal.(submitted)
toward impaired performance during session 2, t(17)=−1.8, found that participants’level of empathy for a familiar charac-
p=0.08. In terms of the ToM events, no significant group dif- terwasmodulatedbytheretrievalofpreviousepisodesinvolving
ferenceemergedforsession1,t(17)=−1.6,p=0.13,orsession thatcharacter.Furthermore,usingthesamefamilyphotospara-
2, t(17)=−0.98, p=0.34. With respect to the EM events, as digmemployedinthecurrentstudy,we(RabinandRosenbaum,
expected, H.C. produced significantly fewer elaborative details 2012)showedthatthepatternofneuralactivitysupportingpToM
thancontrols,t(17)=−1.78,p=0.0473. sharesmoreincommonwithepisodicmemorythanwithToM.
The mean proportion of elaborative-to-total-internal details Notably,thegreatestdegreeofneuraloverlapbetweenpToMand
producedbyparticipantsinresponsetoeachpToM,ToM,andEM episodicmemorywasobservedwithinmidlineregions,including
event is presented in Figure2.Analyses revealed that H.C. pro- thehippocampusandrelatedMTLstructures,regionstraditionally
ducedalowerproportionof elaborativedetails(andthereforea associatedwiththerecollectionofpastevents.
greaternumberofdescriptivedetails)thancontrolsinresponseto Reliance on past personal experiences to infer familiar oth-
thepToMeventsduringbothsession1,t(17)=−7.0,p<0.00001 ers’mental states may occur with or without one’s intention or
and session 2, t(17)=−4.99, p=0.0001. In contrast, H.C. and awareness. There is accumulating evidence that episodic mem-
controlsproducedanequivalentproportionofelaborativedetails orysupportedbythehippocampuscanrapidlyandautomatically
inresponsetotheToMeventsduringbothsession1,t(17)=0.77, influenceperformanceonnon-mnemonictasks(Westmacottand
p=0.45,andsession2,t(17)=−0.32,p=0.75.Consistentwith Moscovitch,2003;Westmacottetal.,2004;Moscovitch,2008;Ryan
our predictions, H.C. generated a lower proportion of elabora- etal.,2008;Greenbergetal.,2009;SheldonandMoscovitch,2010).
tive details relative to controls in response to the EM events, GobbiniandHaxby(2007)suggestthatthemereperceptionofa
t(17)=−2.57,p=0.01. familiar individual is associated with the spontaneous retrieval
ofpersonalknowledgeaboutthatindividual(i.e.,personaltraits,
DISCUSSION
attitudes, biographical facts, and episodic memories), which in
H.C.,adevelopmentalamnesicpersonwithbilateralhippocampal turnmayhelptobetterunderstandandpredictwhatthefamil-
damage,wasimpairedatimaginingtheexperiencesofpersonally iar other is thinking and/or feeling. These automatic processes
mayhavebeenatplayinthecurrentstudygiventhatparticipants
2Duetothesmallnumberofelaborativedetailsproducedforeachevent,wewere wereinstructednottorefertopastepisodeswhengeneratingthe
unabletomakemeaningfulcomparisonswhenthedetailswerefurtherdividedinto pToM and ToM events. It is possible that participants engaged
theinternaldetailcategories(i.e.,event,place,time,perceptual,thought/emotion). ininhibitoryprocessestohelpovercometheprepotenttendency
3Wedidnotconfirmtheaccuracyofparticipants’reportedmemories.However,
torelyonpastmemories.Alternatively,othermemoryregulation
anecdotalevidenceprovidedbyH.C.’sfamilysuggeststhatshetendstofillinmem-
processes, such as thought substitution (Benoit and Anderson,
orygaps.Therefore,H.C.’sEMscoresarelikelyanoverestimateofherepisodic
memorycapabilities. 2012)mayhavebeenemployed.
www.frontiersin.org January2013|Volume3|Article588|5
Rabinetal. Episodicmemoryandimaginingothers’experiences
FIGURE1|ThemeannumberofelaborativedetailsprovidedbyH.C.andcontrolsinresponsetoeachpToM,ToM,andEMevent,*p<0.08;**p<0.05.
Errorbarsindicatestandarddeviations.
FIGURE2|Themeanproportionofelaborative-to-total-numberofinternaldetailsprovidedbyH.C.andcontrolsinresponsetoeachpToM,ToM,and
EMevent,*p<0.01;**p<0.0001.Errorbarsindicatestandarddeviations.
AnotherpossibleexplanationforH.C.’scorrespondingimpair- (Addisetal.,2011;Fordetal.,2011),likelyduetothegreaterrela-
mentinbothepisodicmemoryandpToMmayrelatetoadeficit tionalprocessingthatisrequiredfortheformer(Addisetal.,2011).
in(re)constructingspecificepisodes.Evidencefromneuroimag- Severalresearchershavearguedthatindividualsaremorelikelyto
ing studies suggests that imagining specific versus general past imaginecloseotherswithgreaterspecificityrelativetounknown
andfutureeventselicitsgreateractivitywithinthehippocampus others. In contrast,unknown others are typically represented in
FrontiersinPsychology|Cognition January2013|Volume3|Article588|6
Rabinetal. Episodicmemoryandimaginingothers’experiences
more generic and abstract terms (Liviatan et al., 2008; Lieber- (Lieberman, 2012). Generic representations are likely based on
man,2012).Thismaybebecausewepossessidiosyncratictheories routinesorschemasthatarealreadyboundtogetherandtherefore
aboutcloseothers’personalitiesthatenableustorichlyimagine requireminimalrelationalprocessing.RecentfMRIfindingsfrom
howwell-knownotherswouldrespondinvariousscenarios(see ourlaboratory(RabinandRosenbaum,2012),supportthisinter-
Lieberman,2012). Therefore H.C.’s difficulty in generating spe- pretation. Using the same family photos paradigm, we recently
cificdetailsmayaccountforherpoorperformanceontheepisodic showed that relative to pToM,ToM involving unfamiliar others
memoryandpToMtasks. elicitedgreateractivityinlateralregionsknowntobeassociated
ItmaybethecasethatforthepToMeventsH.C.attemptedto with accessing semantic knowledge (Martin and Chao, 2001).
relyonastrategythatisoptimalforpeoplewhoareabletoconjure Taken together, these data further corroborate the notion that
upcontextualandspecificdetailsratherthanrelyingonastrategy episodic memory may be needed for social cognition, but that
thatwouldbeadvantageousforher.Likecontrols,H.C.mayhave itsrolemaybespecifictoimaginingtheexperiencesofpersonally
beenengagingininhibitoryprocessesofpasteventswhengener- known,andnotunknown,others.
atingthepToMandToMevents.However,becauseherepisodic Theuseofanopen-endedToMtaskallowedustogaininsight
recollectionisimpaired,shemayhavegeneralizedthisinstruction into possible compensatory strategies that H.C. employed when
topersonalsemanticinformation,whichwouldhavelikelyhelped takingtheperspectiveofanotherperson.WefoundthatH.C.gen-
hertogenerateadditionaldetailsforthepToMevents.Itispossible eratedasignificantlygreaterproportionof descriptivedetailsin
thatifshehadbeenprobedinamannerthatenabledhertodraw response to the pToM photos than did controls,suggesting that
moreeffectivelyonherintactpersonalorsocialsemanticmemory, shereliedmoreheavilyonthevisualinformationdepictedinthe
shemayhaveperformedbetteronthepToMtask.Indeed,different photostoimaginetheexperiencesofwell-knownothers.Thismay
methodsofcuingcandifferentiallyaffecttaskperformance.H.C., haveincludedrelyingonthefamiliarother’sfacialexpression,body
forinstance,wasimpairedatimaginingherselfinfutureepisodes language,and/ortherelativespatialrelationsbetweenpeople.This
whenprovidedwithaspecificcueword(e.g.,“coffee”;Kwanetal., strategymayserveherwellinsocialsettingswhenexternalcues
2010)butshowedintactperformancewhenamoregeneraland are readily available but may fail when cues are absent or when
non-specificcuewasprovided(e.g.,“Imaginesomethingyouwill situationsarecomplexandrequiretheintegrationofinformation
bedoingthisweekend”;Hurleyetal.,2011;seealsoCooperetal., fromthepastandpresent.
2011). H.C.’s performance on the pToM condition was not at floor
The corresponding deficit that emerged in episodic memory indicatingthatherabilitytoimaginetheexperiencesof person-
andpToMisunlikelytobeduetoadeficitinnarrativeconstruc- allyfamiliarothersisnotobliterated.Infact,approximately50%
tion,giventhatH.C.hadnodifficultyconstructingnarrativesin ofthedetailsshegeneratedinresponsetothepToMeventswere
responsetotheToMevents.Thispatternof resultsisconsistent elaborative details (i.e., details that go beyond what is visually
withthosefromarecentstudyshowingthattheabilitytogenerate depictedinthephoto).However,uponcloserexamination,even
adetailednarrativeispreservedinadult-onsetamnesia(Raceetal., thequalitativenatureoftheelaborativedetailsshegenerateddif-
2011;butseeRosenbaumetal.,2009).Althoughthepatientsinthe feredfromthatofcontrols.Specifically,H.C.’sresponsestendedto
studybyRaceandcolleaguesproducedimpoverisheddescriptions reflectmorebasicemotionalstatesthatcouldbeinferredfromthe
of pastandfutureevents,theyshowedintactperformancewhen visualfeaturesof thephoto,suchas“they’rebothreallyexcited”
asked to tell a story in response to pictures depicting fictional or“shelooksreallyhappy.”Incontrast,controlparticipantstypi-
characters in various scenes. It is important to note that while callyprovidedmorecomplexmentalstateinferencessuchas“they
theirparticipantswereinstructedtogenerateastoryratherthan were probably afraid but they are trying to look cool”and“her
toreportwhatwasliterallydepictedinthepicture,toourknowl- motherwaspleasedthatherdaughterwashavingsomuchfun”
edge,theauthorsdidnotexaminewhetherparticipantsadheredto (seeFigure3fornarrativesamples).
thisinstruction.Inthecurrentstudy,whenexaminingtheextent H.C. generated a greater number of elaborative details in
towhichparticipantsreliedonthevisualcontentofthephotosto response to the pToM and ToM events during session 2 relative
generate details,we found thatapproximately half of the details to session 1. It is important to note, however, that the overall
H.C.producedforthepToMeventsconsistedofdescriptivedetails pattern remained consistent across the two testing sessions in
(vs.12.5%forcontrols).Thecurrentfindingshighlighttheimpor- that, in both cases, H.C. produced fewer elaborative details for
tanceofexaminingdescriptiveversuselaborativedetailswhenrich the pToM versus ToM events. It is possible that the difference
visualcuesareused. acrosstestingsessionsreflectsapracticeeffectresultingfromexpe-
H.C.’s impairment in episodic memory and pToM contrasts riencewithnarrativegeneration.Althoughourtwotestingsessions
withherpreservedabilitytoimaginetheexperiencesofunknown tookplace3yearsapart,H.C.participatedinseveralotherstud-
othersduringToM.Thelatterfindingisconsistentwithherintact iesthatrequiredhertogeneratedetailednarrativesintheinterim
performanceonawiderangeofstandardToMteststhatemploy (Kwanetal.,2010,2011;Hurleyetal.,2011).Infact,withinthese
strangers or fictional characters as targets (Rabin et al., 2012; other studies, H.C. showed improved performance on tests of
see also Rosenbaum et al., 2007). Imagining the experiences of futureimaginingacrosstestingsessions(Kwanetal.,2010;Hur-
unfamiliar others may be achieved by relying on social seman- ley et al.,2011). A related explanation for H.C.’s inflated scores
tic memory,which remains relatively intact in H.C. This might duringsession2isthatshemayhavelearnedtouseamoreeffec-
include reliance on generic representations about how the aver- tive strategy that enabled her to generate a greater number of
age person is expected to think and feel in a given situation details.
www.frontiersin.org January2013|Volume3|Article588|7
Rabinetal. Episodicmemoryandimaginingothers’experiences
FIGURE3|RepresentativesamplesofthepToM,ToM,andEMnarrativesprovidedbyH.C.andacontrolparticipant.
Inthecurrentstudy,weattemptedtocontrolforvividnessby isunknown(RabinandRosenbaum,2012).Continuedresearch
onlyincludingthepToM,ToM,andEMeventswiththehighest withH.C.andotheramnesicindividuals,particularlythosethat
vividnessratingsinouranalyses.Nevertheless,analysesrevealed acquire damage later in life, is needed to better understand the
thatH.C.ratedthepToMeventsinsession1andtheEMeventsin rolethatepisodicmemoryplaysinthisandotheraspectsofsocial
session2aslessvividthancontrols.Inaddition,wecannotruleout cognition.
thatotherfactors,suchaspersonalsignificance,differedbetween
H.C.andcontrols. ACKNOWLEDGMENTS
In conclusion, using an ecologically valid test of ToM, we This work was funded by a Sloan Research Fellowship,Ontario
formallydocumentthatepisodicmemorysupportedbythehip- Ministry of Economic Development and Innovation Early
pocampus may be pivotal for imagining the experiences of per- ResearcherAward,CanadianInstitutesofHealthResearch(CIHR)
sonallyfamiliar,butnotunfamiliar,others.Thecurrentfindings NewInvestigatorAward,andCIHROperatingGranttoR.Shayna
complementrecentfMRIdataandsuggestthatwhenimagining Rosenbaum (grant MOP 93535),and a CIHR Banting and Best
other people’s experiences individuals are more likely to rely on Doctoral Award to Jennifer S. Rabin. Asaf Gilboa acknowledges
episodic memory when the target person is personally familiar support from the Natural Sciences and Engineering Research
and on general social semantic memory when the target person Council.
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Developmental amnesia: effect of memory.Mem.Cognit.31,761–774. A,StussDTandRosenbaumRS(2013) License,whichpermitsuse,distribution
ageatinjury.Proc.Natl.Acad.Sci. Imagining other people’s experiences andreproductioninotherforums,pro-
U.S.A.100,10055–11060. Conflict of Interest Statement: The in a person with impaired episodic vided the original authors and source
Westmacott,R.,Black,S.E.,Freedman, authors declare that the research was memory: the role of personal famil- are credited and subject to any copy-
M.,andMoscovitch,M.(2004).The conductedintheabsenceofanycom- iarity. Front. Psychology 3:588. doi: rightnoticesconcerninganythird-party
contribution of autobiographical mercial or financial relationships that 10.3389/fpsyg.2012.00588 graphicsetc.
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