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Could an Aging Brain Contribute to Subjective Well-Being?: The Value Added by a Social Neuroscience Perspective

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Could an Aging Brain Contribute to Subjective Well-Being?
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UniversityPressScholarshipOnline
OxfordScholarshipOnline
SocialNeuroscience:TowardUnderstandingthe
UnderpinningsoftheSocialMind
AlexanderTodorov,SusanFiske ,andDeborahPrentice
Printpublicationdate:2011
PrintISBN-13:9780195316872
PublishedtoOxfordScholarshipOnline:May2011
DOI:10.1093/acprof:oso/9780195316872.001.0001
CouldanAgingBrainContributetoSubjectiveWell-Being?
TheValueAddedbyaSocialNeurosciencePerspective
JohnT.Cacioppo
GaryG.Berntson
AntoineBechara
DanielTranel
LouiseC.Hawkley
DOI:10.1093/acprof:oso/9780195316872.003.0017
AbstractandKeywords
Carstensenandcolleaguesreportedthatatleastuntilverylateinlife,healthyolder
adultsreportedlowerlevelsofdepressivesymptomatologyandhigherlevelsof
subjectivewell-being.Thesefindingsweresurprisingnotonlybecausetheywentagainst
socialstereotypesofthemiseryofoldage,butbecausecognitivedeclineswerealso
evidentinolderadults.Carstensenetal.'simportantworkhasledtoeffortstodetermine
theunderlyingcauseoftheage-relateddeclineindepressivefeelingsinthehopesof
Could an Aging Brain Contribute to Subjective Well-Being?
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Chicago; date: 27 Augu st 2014
improvingtreatmentsfordepressivesymptomatologyacrosstheagerange.Earlywor k
focusedonthetemporalperspectiveandself-regulatorystrategiesthatcharacterize
healthyolder adults,butattentiontoage-relatedchangesinbrainfunctionprovidean
alternativeexplanationforthesefindings.Thischaptercontraststhesetwoperspectives
toexaminehowaneuroscientificapproachtoasocialproblemcanproduceinsightsthat
wouldnotbediscerniblefromasocialorbehavioralperspectivealone.Italsoillustrates
thecomplementarynatureofresearchusingfMRIandlesionpatients.
Keywords:aging,socialstereotypes,well-being,depression,oldage,age-relateddecline
WethankHannaDamasioforherassistanceintheanatomicalanalysesoftheneural
lesions.Fu ndingwasprovidedbytheNationalInstituteofAgingGrantNo.PO1
AG18911andtheJohnTempletonFoundation.Corr espondencemaybeaddressed
toJohnT.Cacioppo,CenterforCognitiveandSocialNeuroscience,Universityof
Chicago,5848S.UniversityAvenue,Chicago,IL60637,or
Cacioppo@uchicago.edu.
People’smoodsmodulatesocialcognition,interpersonalinteractions,andsocial
relationships.Forexample,negativemoodscanaltertheperceivedlikelihoodof
occurrenceforconsequencespresentedwhenformingimpressionsorattitudes
(Wegener,Petty,&Klein,1994),andnegativemoodscanhaveadverseeffectson
interper sonalinteractions(Hawkley,Preacher,&Cacioppo,2007).Whenfeelingsof
dysphoriaextendbeyondminutesandhour stoweeksandmonths,theindividual
transitionsfromnegativemoodstodepressivesymptomatology,theconsequencesof
whichcanbedev astating.
Individualswithelevateddepressivesymptomsareatriskforahostofproblems,
includingcardiovasculardisease(e.g.,Barefoot&Schroll,1996;Barth,Schumacher,&
Herr mann-Lingen,2004;Carney&Sheps,2004),functionalimpairments(Mehta,Yaffe,&
Covinsky,2002),diminishedimmunosurveillance(Hawkley,Bosch,Engeland,Marucha,&
Cacioppo,2007),higherhealth-careresourceutilization(Wellsetal.,1989;Wygaard&
Albreksten,1992),socialdisruptions(Cacioppoetal.,2006),andfeelingsofsocialisolation
(Cacioppoetal.,2006).Eventreatmentsfordepressivesymptomscarry significantrisks.
Selectiveserotoninreuptakeinhibitors(SSRIs)areaclassofanti-depressantmedications
thathelpalleviatedepressivesymptomsinmanyindividuals,butthesedrugsadversely
affectosteob lasts(cellsfrombones),resultinginmorebrittlebonesandincreasedriskof
bonefracturesanddisabilityintheelderly(Richard setal.,2007).Whentotaled,the
estimatedannualeconomiccostofdepressivesymptomatologyexceeds$43billion
(Greenber g,Stiglin,Finkelstein,&Berndt,1993).
Depressivesymptomatologyissurprisinglyprevalentinindustrializedcountries.Analyses
fromthefirstwaveoftheHealthandRetirementSurvey(HRS),anationally
representativelongitudinalsurvey,indicatedthatapproximatelyone-thirdofadults
(33.6%ofthoseages51–55yearsand31.2%ofthoseages56–61years)reported
moderatetohighlevelsofdepressivesymptoms(Steffick,2000,Table22).Datafromthe
secondandthirdwaveoftheHRSandthefirsttwowavesoftheAssetsandHealth
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DynamicsStudyoftheOldestOld,inwhichtheCenterforEpidemiologicStudies
DepressionScale(CES-D;Radloff,1977)wasused,indicatedthatfrom14%to19%
respondedthatthey“feltdepressed,”21%to25%respondedthat“everythingwasan
effort,”and17%to23%r espondedthatthey“cou ldnotgetgoing”(Steffick,2000,Table
9).Thesedatasuggestthatdepressive(p.250)symptomatologyhasreachedepidemic
propor tionsandplaysasignificantroleinsocialcognition,interpersonalrelationships,and
socialbehaviorinindustrializednations.Indeed,theFederalInteragencyF or umon
AgingRelatedStatistics(2004)usesdepressivesymptomatologyasanimportantindicator
ofgeneralwell-beingandhealthamongadults.
Withtheagingofindustrializednations,concernsaroseaboutacorrespondingincrease
indepressivesymptomatologyandacompoundingofthehealth-carecostsassociated
withanolderpopulation.Itcameasasurprise,then,whenCarstensenandcolleagues
reportedthatatleastuntilverylateinlife,healthyolder adultsreportedlowerlevelsof
depressivesymptomatologyandhigherlevelsofsubjectivewell-being(e.g.,Carstensen,
Isaacowitz,&Charles,1999).Thesefindingsweresurprisingnotonlybecausetheywent
againstsocialstereotypesofthemiseryofoldage,butbecausecognitivedeclineswere
alsoevidentinolderadults(e.g.,Petersen,Doody,Kurzetal.,2001).Age-r elated
changesincognitionincludeareductioninprocessingspeed,episodicmemory,and
executivefunctioning,includingproblemsolvingandinhibitorycontrol(e.g.,Hasher&
Zacks,1988;Salthouse,2001;Stern&Carstensen,2000;vonHippel&Dunlop,2005).
Moreover,5%oftheUnitedStatespopulationages65to69yearsshowsmoderateor
severememoryimpairment,and32%ofthose85yearsandoldershowmoderateor
severememoryimpairment(FederalInteragencyForumonAging-RelatedStatistics,
2004).
Carstensenetal.’s(1999)importantworkhasledtoeffortstodeterminetheunderlying
causeoftheage-r elateddeclineindepressivefeelingsinthehopesofimproving
treatmentsfordepressivesymptomatologyacrosstheagerange.Earlyworkfocusedon
thetemporalperspectiveandself-regulatorystrategiesthatcharacterizehealthyolder
adults,butattentiontoage-relatedchangesinbrainfunctionprovideanalternative
explanationforthesefindings.Ourgoalinthischapteristocontrastthesetwo
perspectivestoexaminehowaneuroscientificapproachtoasocialproblemcanproduce
insightsthatwouldnotbediscerniblefromasocialorbehavioralperspectivealone.We
alsoillustratethecomplementarynatureofresearchusingfMRI andlesionpatients.
Age-relatedpsychologicalchanges
Cognitivedeclinesareviewedgenerallyastheconsequenceofanagingbrain(e.g.,
McArdleetal.,2004),whereastheimprovedaffectassociatedwithaginghasbeen
attributedtochangesinmotivationderivedfromdifferencesintimeperspective(e.g.,
Carstensen,Fung,&Charles,2003).Accord ingtoCarstensen’ssocio-emotionalselective
theory,peoplehaveasenseoftheirtimeleftinlife,andperceivedboundariesontime
leadstoattentionbedirectedtoemotionallymeaningfulaspectsoflife.Whentimeis
perceivedasabundant,anindividual’smotivationandgoalscenteronacquiringnew
information,expandinghorizons,andpur suingachievements.Whentimeisperceivedto
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belimited,positiveemotionalexperiencebecomesthepreeminentmotivation,andthe
individualtunesattentional,cognitive,andsocialinvestmentstoenhanceemotional
closenessandpositiveaffect.
Thereisconsider ableevidenceconsistentwiththepredictionsofsocio-emotional
selectivity.Inanillustrativestudy,Nolen-HoeksemaandAhrens(2002)investigatedthe
levelsofdepressivesymptomsin25-to35-year-old,45-to55-year-old ,and65-to75-
year-oldadults.Thesegroupswereselectedtorepresentdifferentlifecircumstances
andsocialhistories.Resultsindicatedthatasagroup,theolderadultsrepor tedthe
lowestlevelsofdepressivesymptomatology.
Werecentlyexaminedthedeter minantsofsubjectivewell-beinginourpopulation-based
stud yof50-to67-year-oldsintheChicagoHealth,Aging,andSocialRelationsStudy
(CHASRS;Cacioppoetal.,2006).Consistentwithpriorresearch,ourcross-sectional
analysesindicatedthatdispositionalvariables,suchasemotionalstability,relationship
satisfaction,and self-esteem,wer eassociatedwithsubjectivewell-being.Cross-sectional
analysesmayprovideusefulinformationondispositionalcharacteristicsofhappypeople
aswellasriskfactors;(p.251) longitudinalanalysesaremoreusefultoinvestigatelikely
causalinfluences.Longitudinalanalysesofdatafromthefirst3yearsofCHASRSr evealed
aneffectofageonchangesinsubjectivewell-being,aspredictedbysocio-emotional
selectivitytheory.
Giventhereplicabilityofage-relateddecreasesindepressivesymptomatologyand
increasesinsubjectivewell-being,investigationshavetur nedfromdeterminingthe
associationtoexplicatingtheunderlyingmechanism.Socio-emotionalselectivitytheory
predictsthatolderadultswillself-regulatetheirownaffectivestatesbychoosingto
attendtoandthinkmoreaboutpositive,incontrasttonegative,stimuliandeventsin
their dailylives.Consistentwiththishypothesis,Carstensenandcolleagues(Char les,
Mather,&Carstensen,2003)demonstratedthatage-relateddecrementsinmemory
performancearegreaterfornegativethanpositivestimuli.Recallandr ecognition
memoryforpositive,neutral,andnegativepicturesweremeasuredinyoung(ages18–
29years),middle-aged(ages41–53years),andolderadults(ages76–80years).Results
confirmedthatyoungadultsrecalledcomparablenumber sofpositiveandnegative
stimuli,whereasmiddle-agedandolderadultsrecalledmor epositivethannegative.
However,analternativetosocio-emotionalselectivitytheoryissuggestedbythework
onage-relatedchangesinadrenergicandamygdalafunctioning.Accordingtoanaging-
brainmodel(ABM):(1)theamygdalaactivationinresponsetonegativestimulidecreases
withagewhereasamygdalaactivationtopositivestimuliismaintainedacrossage;(2)the
decreasedamygdalaactivationisassociatedwiththediminutioninemotionalarousalto
negativestimuli;and(3)thediminutionofemotionalarousaltonegativestimulithatis
associatedwithagingcorr espondinglyreducesthememorialadvantageconferredto
emotionallyarousingeventsandelevatessubjectivewell-being.AccordingtotheABM,
thesechangescarryanadditionalcost:themaintenanceoffeltarousaltopositive
emotionaloutcomesandthediminutionoffeltarousaltonegativeemotionaloutcomescan
alsoimpairdecisionmakinginsituationsinwhichweightingnegativefeedbackisessential
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(e.g.,gambling).
TheneuroscientificallyinspiredABMdiffersfromsocio-emotionalselectivitytheoryin
severalrespects.Socio-emotionaltheorypositsthatthegreaterpriorityplacedon
emotionalgoalsbyolderadultsleadsthemtochoosetoattendtoandallocatecognitive
resourcestowardpositive,ratherthannegative,stimuli(e.g.,people,events)asameans
ofmoodregulationandmaintainingemotionalcloseness.AccordingtotheABM,age-
relatedchangesinbrainfunctionincludeimpairmentsinamygdalafunction,whichresults
inreductionsinemotionalimpactofnegative,butnotpositive,stimuli.Bothmodels
predictthatamygdalaactivationwillbecomparabletopositivestimuliinyoungadultsand
willbesmallertonegativethantopositivestimuliinolderadults.Howev er ,socio-
emotionalselectivitytheorypredictsthattheseamygdalachangesaretheconsequenceof
thereducedattentiontoandcognitiveemphasisonnegativeinformationinolder adults
thatcomesfromtheirincreasedfocusonemotionalgoalsandemotionalregulatory
strategies(Carstensenetal.,2003).ABMpred ictsthattheseamygdalachangesarethe
causeofthereducedimpactofnegativestimuliand,consequently,diminisheddepressive
symptomatologyandimprovedsubjectivewell-b eing.
Imagingresearchhasconfirmedthepatternofamygdalaactivationpredictedbysocio-
emotionalselectivitytheoryandbytheABM.Matheretal.(2004)usedevent-related
fMRIinastudyof17healthyyoungadults(ages18–29years)and17olderhealthy
adults(ages70–90years).Theparticipantsviewed192randomlyorderednegative,
neutral,andpositivepicturesfromtheInternationalAffectivePictur eSystem(Lang,
Bradley,&Cuthber t,1999)inadditionto64fixationtrials(alargecrossonthecenterfor
thescreen).Eachofthese256stimuliwerepresentedfor3seconds,andaftereachthe
participantsrated“howexcitedorcalmyoufeelwhenyouvieweachpicture”usinga
scalefrom1to4,with1labeled“completelyr elaxed,calm,sluggish,dull,sleepy,
unaroused”and 4labeled“stimulated,excited,frenzied,jittery,wide-awake,aroused.”
Forold er adults,theaverage(p.252) signalchangeintheamygdalawaslargerfor
positivethannegativepictures,whereasforyoungadultstheaver agesignalchangein
theamy gdalawascomparablylargetopositiv eandnegativepictures.Thatis,young
adultsshowedamygdalaactivationtopositiveandnegativepictures,whereasolder
adultsshowedamygdalaactivationonly inresponsetothepositivepictures.
Furthermore,Matheretal.(2004)foundthatyoungandolderadultsratedthepositive
picturesascomparablyemotionallyarousing,butolderadultsratedthenegative
picturesaslessarousingthandidtheyoungadults.
TheresultsofMatheretal.(2004)andCharlesetal.(2003)areconsistentwith
Carstensen’ssocio-emotionalselectivitytheorywhereinolderadultspreferemotionally
meaningfulexperiences,andthisincreasedfocusonemotionalgoalsandemotional
regulator ystrategiesleadstoareducedcognitiv efocusonnegativeinformation.Their
resultsarealsoconsistentwiththeABM,whereinthereducedamygdalaactivationin
older,comparedtoyoung,adultsfoundinresponsetonegativ e(butnotpositive)stimuli
isanage-relatedchangeinbrainfu nctionandiscausal:theloweramygdalaactivation
shownselectivelytonegativestimulidrainsthemofemotionalarousal,which,asCahilland
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colleagues(1994,1995)haveshown,eliminatesthememorialadvantageusuallyfoundfor
emotionalstimuli.
Socio-emotionalselectivitytheoryandABMdifferintheirpredictionsaboutattentionto
negativeversuspositivestimuli.Basedontheformer ,Charlesetal.(2003,Study2)
hypothesizedthat“olderadults,comparedwithyoungeradults,wouldspendlesstime
viewingthenegativeimagesthanpositiveimages”(p.319)intheirworkofagingand
emotionalmemory.Contrarytosocio-emotionalselectivitytheoryandconsistentwiththe
ABM,however,Charlesetal.(2003)foundthatbothyoungandoldadultsspentmore
timeviewingnegativethanpositivestimuli,andnodifferencesbetweenyoungandold
adultswerefoundinthetimespentviewingnegative(or positive)images.
Theextantdataareallcorrelationalinnature,andtheydonotaddr esswhethertheage-
relatedchangesinamygdalafunctionobser vedintheliteratur e:(1)aretheconsequence
ofchangesintheperceivedtimeleftinlife,whichmotivateschangesintheattentionto
andcognitiveoperationsonpositiveandnegativeinformation(thesocio-emotional
selectivityprocess-hypothesis),or(2)lessentheemotionalar ousalelicited specificallyby
negativestimuli,which,inturn,producesaneffectivelandscapeinwhichpositiveand
negativestimuliarerecognizedassuchbu tinwhichpositivestimuliareassociatedwith
greateremotionalarousal(andgreatermemorialandgeneralaffectiveimpact)than
negativestimuli(theABMprocess-hypothesis).OneofthefundamentaltenetsoftheABM
isthatpatientswithamygdala/anter iortemporallesions,evenyoungpatientswithsuch
lesions,willbeselectivelyimpairedinthearousalresponsetonegativestimuli.This,of
course,isbecauseamygdalafunctionisseenascauseratherthanconsequence.The
investigationofpatientswithselectivelesionsoftheamygdala/anteriortemporalregions
ratherthanfMRIstudiesofyoungandoldadultspermitsthebettertestofthis
hypothesis.
Amygdalalesionsandemotionalarousal
Totestthetenetthatpatientswithamygdala/anteriortemporallesionswillbeselectively
impairedinthefeltarousalelicitedbynegativestimuli,Berntson,Bechara,Damasio,
Tranel,andCacioppo(2007)examinedtheseparatevalenceandarousalaspectsof
evaluativejudgmentsinthecontextofacomprehensiv eevalu ativespacemodel
(Cacioppo&Berntson,1994).Specifically,wecomparedtheaffectiveratings(positiv ity,
negativity,andarousal)ofgradedemotionalpicturestimuli(verypositive,moderately
positive,neutral,moderatelynegative,andverynegative;InternationalAffectivePicture
Series[IAPS],Langetal.,1999)by sixpatients(fourmalesandtwofemales;ages22–65
years,mean=37.8)withamygdala/anteriortemporallesionstotheratingsofalesion
controlgroup(threemalesand threefemales;ages33–61years,mean=51.2)with
lesionssparingtheamygdalaandotherareasthathavebeenimplicatedin(p.253)
emotionalprocesses(e.g.,ventromedialprefrontalcortex,insula/SSII;Berntsonetal.,
2006).Resultswerealsocomparedtoalargesetofnormativedataonthesepictures
(Lang,Bradley,&Cuthbert,1999).Participantsratedeachof48picturesonafive-point
bivariatescaleofpositivityandnegativity,andaunivalentscaleofarousal.Pictureswere
matchedonevaluativeextremityfromthemid(neutral)-pointofthenormativescale(12
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verypositive,6moder ately positive,12neutral,6moder ately negative,and12very
negative)and normativearousalratings.Pictureswerepresentedinrand omorderona
computermonitorfor6seconds.Participantswereinstructed tofocusontheemotional
contentofthepicturesandtoratethemonpositivityandnegativitybymovingamouse
pointer andclickingalocationina5(positivity,0=notatall,4=extremely)x5
(negativity,0=notatall,4=extremely)gridpresentedonthescreenimmediatelyafter
terminationoftheslide(Cacioppoetal.,2004).Immediatelyafterresponding,asecond
screendisplayedasingle-responsecontinuum,andtheparticipantwasinstructedtorate
thearousabilityofthestimulus(0–4;0=notatall,4=extremely),againbytheuseofa
mouse.Threesecondsaftercompletingtheratings,thenextslidewaspresented.In
additiontotheseparateratingsofpositivity,negativity,andarousal,anetvalencerating
wascalculatedasthepositivityratingminusthenegativityratingforeachpicture.
AsillustratedFigure17–1,theamygdala/anteriortemporalgroupshowedmarkedly
reducedarousalratingstonegativeemotionalstimuli,despiteratingsofneutraland
positivestimulithatwerehighlysimilartothoseoftheclinicalcontrolgroupandtoa
normativeadultsample(Langetal.,1999).Ananalysisofvariance,withpolynomialtrends
analysis,revealedasignificanteffectofpicturecategory(verypositive,moder ately
positive,neutral,moderatelynegative,ver ynegative)onarousalratings,characterized
byasignificantoverallquadratictrendacrosspicturecategories.Thelatter reflectsthe
minimalarousaltoneutralstimuliandtheprogressivelyincreasingarousaltoeither
positiveornegativestimuli,ashasbeenreportedpreviously.Therealsoemergeda
significantgroupx
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Fig.17–1 Arousalandvalenceratings.Mean(s.e.m.)arousal(A)
andvalence(B)ratingsacrossstimuluscategories,forpatientswith
amygdalalesions(Amyg)comparedtotheclinicalcontrastgroup
(Cnt)andnormativecontroldata(Norm).Allgroupseffectively
discriminatedthestimuluscategoriesandappliedvalanceratings
accordingly.Allgroupsalsodisplayedcomparablearousalfunctions
topositivestimuli,buttheamygdalagroupshoweddiminished
arousalselectivelytothenegativestimuli.(FromBerntson,G.G.,
Bechara,A.,Damasio,H.,Tranel,D.,&Cacioppo,J.T.[2007].
Amygdalacontributiontoselectivedimensionsofemotion.Social,
Cognitive,andAffectiveNeuroscience,2,123–129.)
(p.254)picture-categoryinteraction,characterizedbyasignificantdifferencebetween
thegroupsinthelineartrendcomponentacrosspicturecategories.Thisreflectedthe
reducedarousalratings,selectivelyforthenegativepictures,bytheamygdala/anterior
temporalgroup.Incontrasttotheclinicalcontrolgroupandthenormativegroup,the
amygdala/anteriortemporalgroupdisplayedminimalarousalratingstonegativepictur e
content.
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Animportantquestionarisesastowhetherthediminishedarousaltonegativestimuliin
theamy gdala/anteriortemporalgroupmaybeattributabletoimpairedrecognitionor
discriminativeprocessingofthenegativ efeaturesofthepictures.AsillustratedinFigure
171B,however,theamygdala/anteriortemporalgroupwasabletocategorizeandlabel
thenegativepicturecontentaccurately,suggestingafundamentaldissociationbetween
thecognitiv eandaffectiveprocessingofthestimuliinthisgroup.Analysisofvariance,
withpolynomialtrendsanalysis,revealedtheexpectedsignificanteffectsofpicture
categoryonpositivityratingsandnegativityratings,eachbeingcharacterizedbya
significantlinearcomponent(forpositivityratingsandfornegativity).Therewereno
significantmaineffectsorinteractionsforgrouponeitherpositivityornegativityratings,
althoughforpositivityratings,aninteractiononthelinearcomponent,reflectingthe
somewhathigherslopeofthepositivity-r atingfunctionoftheamygdala/anter iortemporal
group,approachedsignificance.
Twopatientsintheamy gdala/anteriortemporalpatientshadabilaterallesion,andfour
hadunilaterallesions.Bilateralamygdalalesionshavegenerallybeenfoundtoyield larger
effectsthanunilaterallesions,althoughunilaterallesionshavebeenreportedtohave
similaralthoughattenuatedeffects(Glascher&Adolphs,2003;LaBar etal.,1995;Phelps
etal.,1997)or,insomecases,evencomparableeffectstobilaterallesions(Buchananet
al.,2004).Weexaminedthisissueinfurtheranalysesofthechangeinresponse(from
neutral)topositiveandtoneutralstimuliinbilateralandunilateralpatients.
AsillustratedinF igure172,thelesioncontrolgroupevid encedasomewhatgreater
arousalresponsetonegativestimulithantopositivestimuli,whereasthereversepattern
wasappar entfortheamygdala/anteriortemporalgroup.Ananalysisofvariancerevealed
asignificantgroupxpicture-category(positive/negative)interactiononarousalratings.
Thisinteractionwasattributabletothesimilararousalresponsesofthegroupstopositive
stimuli,andtheconsiderablysmallerresponsesoftheamygdala/anteriortemporalgroup
tonegativestimuli.
Figure17 2alsorevealsdifferencesinthearousalresponseofpatientswithbilateraland
unilateralamygdala/anteriortemporallesions.Thearousalresponseofthebilateral
patientstonegativestimuliweresmallerthanthoseofunilateralparticipants,buteven
thosewithunilaterallesionsshowedasubstantialattenuationofarousaltonegative
stimuli.
Thepresentfindingsindicatethatpatientswithamygdala/anteriortemporallesionsarenot
impairedatrecogniz ingandlabelingnegative
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Fig.17–2 Effectsofbilateralandunilaterallesions.Heavybarsshow
overallmean(s.e.m.)ofthechangeinarousalratingstopositiveand
negativestimuli,comparedtoneutralstimu li,forpatientswith
amygdaladamageandclinicalcontrast(Control)subjects.Lighter
barswithintheheavybarsoftheAmygdalagroupillustrateeffects
ofunilateralvs.bilaterallesions.(FromBerntson,G.G.,Bechar a,A.,
Damasio,H.,Tranel,D.,&Cacioppo,J.T.[2007].Amygdala
contributiontoselectivedimensionsofemotion.Social,Cognitive,
andAffectiveNeuroscience,2,123–129.)
(p.255)aswellaspositiveemotionalcontentinpictures.Theyarealsocapableof
emotionalarousal,asevidencedbytypicalarousalfunctionstopositiveemotionalstimuli.
Incontrast,however,theydisplayanattenuatedarousaltonegativeemotionalstimuli.
Theseresultsareconsistentwithpreviousreportsofdiminishedarousaltonegative
stimuliinpatientswithamygdalalesions(Adolphs,Russell,&Tranel,1999;Winstonetal.,
2005)bu textendthesefindingsbyshowingthatthisarousaldeficitdoesnotarisefroma
cognitive/perceptualdeficitinrecogniz ingandlabelinggradednegativepicturecontent
(seealsoAdolphsetal.,1999).
Neithermemorynordepressivesymptomatologywasmeasur edinthispreliminary
stud y,butthesedataindicatethatamygdaladamagecausesreducedemotionalarousal
specificallytonegativestimuli.Giventhiseffect,itisfeasiblethatthememorialbenefit
typicallycharacteristicofnegativestimuliisdiminishedinindividualswithamygdala
damage,andrelatedlythereducedemotionalimpacttoandmemoryfornegativeevents
lessensdepressivesymptomatologyandmayimpair decisionmakingwhenconsequences
arenegative.Thishypothesiswarrantsfurtherinvestigation.
Wehavefurthersuggestedthatagingmaybeassociatedwithareductioninamy gdala
function,leavingolderadultstoevincecognitiveandaffectiveeffectssimilartothose
shownbymiddle-agedpatientswithamygdaladamage.Thepatientswithamygdala
damageandthelesioncontrolswhosedataareshowninFigures17–1and17–2were
selectedtobematchedongenderandage.Inaddition,Berntsonetal.(2007)identified
twopatientsolderthanage80yearswithdamagethatsparedtheamygdala/anterior
temporalregion.Figure17–3presentstheresultsforthearousalr atings.Thefive
categoriesofimagesalongthex-axisareverypositive,moderatelypositive,neutral,
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moderatelynegative,andverynegative,andtheirarousalr atingsaredepictedalongthe
ordinate.Thedottedlinerepresentsthenormativeratingsobtainedfrom
undergraduates,thedashedlinerepresentsthemeanratingsofemotional
Fig.17–3 Ageandarousalratings.Mean(s.e.m.)arousalratings
acrossstimuluscategories,fortwoelder lypatientswithlesions
sparingtheamygdalaandregionsimplicatedinemotion(SS80)
compar edtotheclinicalcontrastgroup(Cnt)andnormativ econtrol
data(Norm).
arousalbymiddle-agedlesioncontrols,andthesolidlinerepresentsthemeanratingsof
emotionalarousalbythetwoelderlylesionpatients.Thearousalratingsfromtheelderly
patientslooksimilartothoseobtainedfromthemiddle-agedpatientswithamygdala
damage.Althoughpreliminary,thesedata,togetherwiththeinvestigationsusingfMRI
showingthattheamygdalaactivationobser vedinyoungadultstonegativeor threatening
stimuliarereducedor absentinolderadults(e.g.,Gunning-Dixonetal.,2003),fitthe
notionthatage-relatedbrainchangesincludereductionsinamygdalafunction,whichin
turnleadstoreducedemotionalarousalspecificallytonegativestimuliand,consequently,
toreducedemotionalimpacttoandmemoryfornegativeevents.Ifthisisthecase,
reduceddepressivesymptomatologyandimproved subjectivewell-beingcouldeasilybe
conceivedtofollow(Wood&Conway,2006).
Insum,workontheagingbr ainsuggeststhereisashiftfromtheamygdala-hippocampal
systemtotheprefrontalcortexovertime(Leigland,Schulz ,&Janowsky,2004).Thisshift
maybemorenuancedthanpreviouslythought,however,withdiminishedamygdala
functionmoreevidentinresponsetonegativethanpositivestimuli,andwith
consequencesforaffect,cognition,andsocialbehaviorthathavemoreincommonthan
previouslyappreciated.Preliminaryevidenceforthisimplicationwas(p.256)recently
reportedbyWilliamsetal.(2006)intheneurosciences.
Conclusion
Therehavebeentremendousadvancesinourunderstandingofthelinksbetweenthe
mind,brain,andbehavioroverthepastquarter centur y,butpeoplehavegenerallybeen
consideredasisolatedunitsintheseanalyses.Peopleareinherentlysocialcreatures,
however,andthetoolsarenowavailabletodeterminethebiologicalmechanisms
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underlyingsocialcognition,emotion,andinterpersonalinteractions.Discoveringthe
biologicalmechanismsunder lyingsocialandaffectiveprocessesandbehav ioris
undoub tedlyoneofthemajorprob lemsfortheneurosciencestoaddressinthetwenty-
firstcentury.
Anassumptionunderlyingsocialneuroscienceisthatallhumansocialbehavioris
implementedbiologically.Thegenerativepowerofsocialneur osciencecomesinpar tfrom
afocusonfundamentalmechanismsandprocesses,suchasage-relatedchangesinbr ain
function,andfromthederivationofnovelandtestablepred ictionsaboutcommon
underlyingmechanismsforwhatappeartobedisparateeffects.Wehaveattemptedto
illustratethesepointsinthecurrentchapter.Age-relatedimprovementsinsubjective
well-beingandage-relateddecrementsincognitivefunctioninganddecisionmakinghave
beentreatedinitiallyasseparateeffects.Theseeffectswerediscoveredindisparate
fieldsandcontinuetoberegarded bymanyasunrelatedchangesassociatedwithaging.
Althoughwedonotmeantosuggestthatallage-r elatedmemoryimpairments,decision-
makingproblems,andmoodimprovementsderivefromasinglecause,age-related
changesinamygdalafunctioningmaycontributetoeach.Basedonadevelopingmodelof
theneuralorganizationofevaluativeprocessesandanimalandhumanr esearchonthe
contributionofspecificneuralsubstratestovalencejudgments,wereasonedthatthe
amygdalacomplexisimportantinaffectiveprocessingofnegativelyvalencedstimuliand
specificallythatamygdaladamageisassociatedwiththereductionofemotionalarousal
elicitedbynegativebutnotneutralorpositivestimuli.Reductionsinemotionalarousal
arecommonplaceinaging,andwereasonedthatbothamygdalaactivationandthe
emotionalarousalelicitedby negativestimuliarelowerinolderadultsthaninyoung
adults.Inaccordwithpriorworkshowingthatemotionalarousalpromotesmemoryfor
emotionalevents,wefurtherreasonedthatthered uctionintheage-relatedchangesin
amygdalaactivationandemotionalarousaltonegativeeventsisassociatedwithpoorer
memoryfortheseevents,greaterreductionsinoverallnegativeaffect(i.e.,improved
subjectivewell-being),andimpaireddecisionsincircumstancesthatrequirethe
considerationofnegativeinformation.Theextantevidenceisconsistentwiththisanalysis,
butadditionaldataarerequiredtotestrelatedpredictionsoftheABM .
Whetherornotthismodelprovestobecorrectislessimportantherethanitsoriginsin
theneuroscienceliterature,itssuggestionthatwhatappeartobedisparateeffectsin
socio-emotionalprocessesmayhaveacommonunderlyingcause,itsverydiffer ent
explanationfromsocio-emotionalselectivitytheoryforage-relatedchangesinsubjective
wellbeing,itsintegrationofdatafrommultiplelevelsoforganization(e.g.,neurochemical,
brain,affect,cognition,andsocialbehavior),itsgenerativenessandfalsifiab ility,andits
demonstrationofthecomplementaryrolesplayedbylesionandimagingresearch.
Indeed ,thevalueaddedbyasocialneuroscienceperspectiveisthatnovel,testable
hypothesesforcomplexsocialprocessesandbehaviorsarenotonlypossiblebutnatural.
Asaconsequence,thisper spectivepullstogetherliteratures,techniques,and
investigatorsfromscientificdisciplinesthatwereoncethoughttohavenothingin
common.
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Thesedevelopmentsarenomoreathreattotraditionalsocialpsychologicalandsocial
scienceapproachesthantheproposedmodelisathreattosocio-emotionalselectivity
theory.Thetwomodelsareincompatibleinsomerespects(e.g.,theroleoftheamygdala),
butevidencefortheABMdoesnotmeanthatsocio-emotionalselectivitytheorycannot
alsooperateinsomecircumstances,andviceversa.Indeed,(p.257) Carstensenand
Fredrikson(1998)demonstratedthattheregulationofemotionalstatesandthe
consequentimprovementsinaffectarenotlimited toolderadults;youngeradultswho
areapproachingtheendoflifeshowsimilarmotivationaladjustments.Thisresult
suggestsbothprocessesmaycontributetoimprovementsinsubjectivewell-beinglater
inlife.
Finally,anassumptionunderly ingsocialneuroscienceisthatallhumansocialbehavioris
implementedbiologically.Itdoesnotfollowthattheconceptsofbiologycanby
themselvesdirectlydescribeorexplainsocialbehaviororthat“molecular”formsof
representationprovidetheonly orbestlevelofanalysisforunder standinghuman
behavioror mentaldisorders.Scientificconstru ctsdevelopedbybehavioralandsocial
scientistsprovideameansofunderstandinghighlycomplexactivitywithoutneedingto
specifyeachindividualactionbyitssimplestcomponents,thereby providinganefficient
approachtodescribingcomplexsystems.Moreimportantly,thereareconceptsessential
tothedescriptionandunderstandingofsocialbehaviorthatarenotcontainedinbiology.
Byanalogy,chemistswhoworkwiththeperiodictableonadailybasisuserecipesrather
thantheperiodictabletocook,notbecauseaparticularfoodpreparationcannotbe
codedbycomplexchemicalexpressions(Cacioppoetal.,2000).However,efficiencyof
expressionisnottheonly issue:theconceptsdefiningfinecuisinearenotpartofthe
disciplineofchemistry.Thetheoreticaltermsofthebehavioralandsocialsciencesare
similarlyvaluableinrelationtothoseofbiologybutcanbeinformed,complemented,and
refinedthroughintegrationwiththeoriesandmethodsfromtheneurosciences.
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... This positivity bias in older adults is controversially discussed with regard to scope and explanation [43,47]: Socio-emotional selectivity theory [48] assumes that older adults intentionally focus more on positive rather than negative experiences as compared to younger adults [45]. In contrast deterioration-based accounts lead positivity bias back to specific or more general neural decline [49,50]. In any case, reduction of negative affect might also occur for emotional responses to touched materials. ...
... One may wonder whether these changes could, alternatively, be explained by changes in emotional responses. However, literature suggests that negative, but rather not positive experiences are reduced in older adults [43][44][45][46][47][48][49][50], rendering this explanation unlikely, because granular materials elicits positive feelings. ...
... As well it is surprising that the inverse relation between valence and roughness is preserved into older age. Note that this is also against the typical trend of reduced processing of negative feelings (for instance, disgust, fear) in older age [43][44][45][46][47][48][49][50]. Though, in a previous study on relearning valences [56], we found that the valence of granular materials could be unlearned in young adult participants but not that of rough material. ...
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In everyday interaction we touch different materials, which we experience along a limited number of perceptual and emotional dimensions: For instances, a furry surface feels soft and pleasant, whereas sandpaper feels rough and unpleasant. In a previous study, younger adults manually explored a representative set of solid, fluid and granular materials. Their ratings were made along six perceptual dimensions (roughness, fluidity, granularity, deformability, fibrousness, heaviness) and three emotional ones (valence, arousal, dominance). Perceptual and emotional dimensions were systematically correlated. Here, we wondered how this perceptuo-affective organization of touched materials depends on age, given that older adults show decline in haptic abilities, in particular detail perception. 30 younger participants (~22 years, half females) and 15 older participants (~66 years) explored 25 materials using 18 perceptual and 9 emotional adjectives. We extracted 6 perceptual and 2 emotional dimensions. Older and younger adults showed similar dimensions. However, in younger participants roughness and granularity judgments were done separately, while they were collapsed in a single dimension in older people. Further, age groups differed in the perception of roughness, granularity and valence, and older people did not show a positive correlation between valence and granularity as did younger people. As expected, control analyses between young males and females did not reveal similar gender differences. Overall, the results demonstrate that older people organize and experience materials partly differently from younger people, which we lead back to sensory decline. However, other aspects of perceptual organization that also include fine perception are preserved into older age.
... (e.g., emotion processing regions in the brain; Cacioppo et al., 2011;Raz et al., 2005) and cognitive changes in attention, memory and processing speed (Glisky, 2007), which can influence how they decode emotional cues (Ruffman et al., 2008). Age-related emotional changes are also linked to unique life experiences and socialization processes with advancing age (Magai et al., 2006). ...
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Sex differences in verbal and nonverbal emotion processing in older individuals are underexplored despite declining emotional performance with age. This study aimed to investigate the nature of sex differences in age-related decline in emotion perception, exploring modulatory effects on communication channels and emotion categories. Seventy-three older adults (43 female participants, aged 60–89 years) and 74 younger adults (37 female participants, aged 18–30 years) completed a task to recognize basic emotions (i.e., anger, happiness, neutrality, sadness) expressed by female or male encoders through verbal (i.e., semantic) and nonverbal (i.e., facial and prosodic) channels. Female participants consistently demonstrated an overall advantage in emotion perception and expression across both age cohorts. In older adults, this superiority was heightened in decoding angry and sad faces, as well as angry prosody and happy and sad semantics. However, older individuals exhibited decreased sensitivities to angry semantics, sad prosody, and neutral prosody from female encoders, whereas they showed heightened sensitivities to happy faces from female encoders and angry faces from male encoders. Both older and younger adults displayed age-related changes in sex interactions specific to emotional categories and channels. But neither own-sex nor opposite-sex bias was systematically observed across the two age groups. These results suggest that explicit emotion processing involves an intricate integration of individual and contextual differences, with significant age and sex interplay linked to specific emotions and channels.
... Older adults may be inclined to depend on compensatory responses to offset cognitive decline (Gruhn et al., 2005;Grühn et al., 2007;Leclerc & Kensinger, 2008). As the ability to process negative affect and information may also decline with age (Cacioppo et al., 2011), it is reasonable to expect that older adults are more likely to engage in gaze reinstatement (as a compensatory strategy) when processing negative visual stimuli compared to younger adults. ...
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Objectives Although research has shown that the replay of encoding-specific gaze patterns during retrieval, known as gaze reinstatement, facilitates memory retrieval, little is known about whether it differentially associates with the negativity preference in memory (defined as enhanced memory for negative stimuli relative to neutral stimuli in this study) among younger and older adults. The present study aims to address this research gap. Methods A total of 33 older adults (16 women; aged 58–69 years, M = 63.48, SD = 2.98) and 36 younger adults (10 women; aged 18–26 years, M = 20.39, SD = 1.57) completed a remember/know recognition memory task involving negative and neutral pictures. Their eye movements were tracked during both the memory encoding and retrieval phases. Results Younger and older adults had better memory for negative than neutral pictures. Older adults exhibited significantly stronger gaze reinstatement for negative than neutral stimuli, while this difference was nonsignificant in younger adults. Moreover, gaze reinstatement is positively linked to memory performance in both age groups. Discussion The results suggest that gaze reinstatement may play age-differential roles in the negativity preference of memory. Negative valence may enhance gaze reinstatement, which improves subsequent recognition memory, particularly among older adults. The finding contributes to a better understanding of the mechanisms underlying the negative preference for memory in different age groups.
... Carstensen and DeLiema, 2018). While Cacioppo et al. (2011) argue that this effect roots in age-related brain changes, others assume that it results from the use of cognitive-control techniques (Kryla-Lighthall and Mather, 2009;Nashiro et al., 2012). Nevertheless, the positivity effect could explain why age-related decline in happiness recognition is rather small compared to negative emotions (Ruffman et al., 2008;Hayes et al., 2020). ...
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Neuroscientific research on emotion has developed dramatically over the past decade. The cognitive neuroscience of human emotion, which has emerged as the new and thriving area of 'affective neuroscience', is rapidly rendering existing overviews of the field obsolete. This handbook provides a comprehensive, up-to-date and authoritative survey of knowledge and topics investigated in this cutting-edge field. It covers a range of topics, from face and voice perception to pain and music, as well as social behaviors and decision making. The book considers and interrogates multiple research methods, among them brain imaging and physiology measurements, as well as methods used to evaluate behavior and genetics. Editors Jorge Armony and Patrik Vuilleumier have enlisted well-known and active researchers from more than twenty institutions across three continents, bringing geographic as well as methodological breadth to the collection. This timely volume will become a key reference work for researchers and students in the growing field of neuroscience.
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Objectives: The purpose of this study was to identify differences between younger and older adults in emotional valence (EV) of words produced during the first and second halves of a 1-minute verb fluency (VF) task. We also sought to determine the relationships between EV, demographic information, VF performance, working memory (WM), and Korean-Mini Mental State Examination (K-MMSE).Methods: A total of 62 healthy individuals participated in the study, with 31 individuals in each age group. A VF-task was conducted for a 1-minute window. The ratios of positive or negative verbs were calculated for the first and second halves of the task period. Digit forward and backward tests were administered and treated as a single index of WM capacity.Results: Both groups produced significantly more positive-EV words than negative, and in the first 30s compared to last 30s. The older adults produced significantly more positive-EV words in the first 30s than the younger group. The positive-EV ratio of verbs in the first 30s showed a significant negative correlation with task performance, K-MMSE, and WM measure. It also showed significant positive correlation with participants’ age.Conclusion: The current study indicates a significant decline in word production rate over time, and a tendency of easily producing positive-EV words in both group. Furthermore, the study revealed the elderly’s positivity effect on task performance. Lastly, using more positive-EV words in the early period of task tendency was significantly and negatively correlated with the task performance, WM measures, and K-MMSE.
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Evaluative processes refer to the operations by which organisms discriminate threatening from nurturant environments. Low activation of positive and negative evaluative processes by a stimulus reflects neutrality, whereas high activation of such processes reflects maximal conflict. Attitudes, an important class of manifestations of evaluative processes, have traditionally been conceptualized as falling along a bipolar dimension, and the positive and negative evaluative processes underlying attitudes have been conceptualized as being reciprocally activated, making the bipolar rating scale the measure of choice. Research is reviewed suggesting that this bipolar dimension is insufficient to portray comprehensively positive and negative evaluative processes and that the question is not whether such processes are reciprocally activated but under what conditions they are reciprocally, nonreciprocally, or independently activated. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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In this article, we attempt to distinguish between the properties of moderator and mediator variables at a number of levels. First, we seek to make theorists and researchers aware of the importance of not using the terms moderator and mediator interchangeably by carefully elaborating, both conceptually and strategically, the many ways in which moderators and mediators differ. We then go beyond this largely pedagogical function and delineate the conceptual and strategic implications of making use of such distinctions with regard to a wide range of phenomena, including control and stress, attitudes, and personality traits. We also provide a specific compendium of analytic procedures appropriate for making the most effective use of the moderator and mediator distinction, both separately and in terms of a broader causal system that includes both moderators and mediators. (46 ref) (PsycINFO Database Record (c) 2012 APA, all rights reserved)
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Modern neurosurgical concepts call for not only "seeing" but also for "localizing" structures in three-dimensional space in relationship to each other. Hence there is a need for a reference system. This book aims to put this notion into practice by means of anatomical and MRI sections with the same stereotaxic orientation. The purpose is to display the fundamental distribution of structures in three-dimensional space and their spatial evolution within the brain as a whole, while facilitating their identification; to make comparative studies of cortico-subcortical lesions possible on a basis of an equivalent reference system; to exploit the anatomo-functional data such as those furnished by SEEG in epilepsy and to enable the localization of special regions such as the SMA in three-dimensional space; and to apply the anatomical correlations of this reference system to neurophysiological investigations lacking sufficient anatomical back-up (including PET scan).