Functional imaging studies of emotion regulation

24 Pages·2012·1.01 MB·English

Ann.N.Y.Acad.Sci.ISSN0077-8923
ANNALS OF THE NEW YORK ACADEMY OF SCIENCES
Issue:TheYearinCognitiveNeuroscience
Functional imaging studies of emotion regulation:
a synthetic review and evolving model of the cognitive
control of emotion
KevinN.Ochsner,JenniferA.Silvers,andJasonT.Buhle
DepartmentofPsychology,ColumbiaUniversity,NewYork,NewYork
AddressforCorrespondence:KevinOchsner,DepartmentofPsychology,ColumbiaUniversity,369SchermerhornHall,1190
AmsterdamAve.,NewYork,[email protected]
Thispaperreviewsandsynthesizesfunctionalimagingresearchthatoverthepastdecadehasbeguntooffernew
insightsintothebrainmechanismsunderlyingemotionregulation.Towardthatend,thefirstsectionofthepaper
outlinesamodeloftheprocessesandneuralsystemsinvolvedinemotiongenerationandregulation.Thesecond
sectionsurveysrecentresearchsupportingandelaboratingthemodel,focusingprimarilyonstudiesofthemost
commonly investigated strategy, which is known as reappraisal. At its core, the model specifies how prefrontal
andcingulatecontrolsystemsmodulateactivityinperceptual,semantic,andaffectsystemsasafunctionofone’s
regulatorygoals,tactics,andthenatureofthestimuliandemotionsbeingregulated.Thissectionalsoshowshowthe
modelcanbegeneralizedtounderstandthebrainmechanismsunderlyingotheremotionregulationstrategiesaswell
asarangeofotheralliedphenomena.Thethirdandlastsectionconsidersdirectionsforfutureresearch,including
howbasicmodelsofemotionregulationcanbetranslatedtounderstandchangesinemotionacrossthelifespanand
inclinicaldisorders.
Keywords: amygdala;cognitivecontrol;emotion;emotionregulation;prefrontalcortex
...Thyfateisthecommonfateofall, Suchstrategiesallowustowhollyorpartiallyalter
Intoeachlifesomerainmustfall... the nature, magnitude, and duration of our emo-
HenryWadsworthLongfellow tional responses, including initiating new ones. In
TheRainyDay(1842) recentyears,greatstrideshavebeentakeninusing
neurosciencetechniquestounderstandthemecha-
...‘Everycloud,’saystheproverb,‘hasasilver
nisms underlying emotion regulation. In humans,
lining.’
thisresearchhasprimarilyusedfunctionalimaging
P.T.Barnum
toexamineourabilitytocontrolaffectiveresponses
StrugglesandTriumphs(1869)
usingcognitivestrategies.Theoverarchinggoalsof
It might be said that emotions are the weather of thispaperaretoreviewtheprogressmadebysuch
ourlives.Somedays,weexperiencetheblueskiesof research,synthesizefromitconclusionsthatsuggest
happinessandthesunshineofjoy.Otherdays,weare expansion on and elaborations of a model of the
drenchedbytheraincloudsofsadnessorbuffeted cognitive control of emotion (MCCE), and show
bythehotwindsofanger.Howwerespondadap- how the model can make sense of a wide range of
tively to our emotional weather patterns—finding emotionregulatoryabilitiesandalliedphenomena.
the silver lining in every dark cloud—has impor- Towardtheseends,theremainderofthepaperis
tantconsequencesforourphysicalandmentalwell- dividedintothreeparts.Inthefirst,weoutlineaba-
being.1–7 sicMCCEwhosecoreelementshavebeendescribed
Althoughwecannotcontroltheweatheroutside, previously.9,10Inthesecondsection,wereviewcur-
wearecapableofusingmyriademotionregulation rentimagingresearchsuggestingwaysinwhichthe
strategiestotakecontrolofourinternalclimates.8 model canevolveto integrate newfindings onthe
doi:10.1111/j.1749-6632.2012.06751.x
Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences. E1
Functionalimagingstudiesofemotionregulation Ochsneretal.
Withthisinmind,ourreviewofcurrentresearch
willsometimesbeorganizedintermsofphenomena
describedatthelevelofbehavior,includingregula-
torygoals,tactics,andtargetstimuli.Inothercases
itwillbeorganizedintermsofissuesconcerningthe
neural-levelpathwaysonwhichthefieldhasbegun
tomakeprogress.Takentogether,thedatareviewed
ineachsectionconstrainsandinfluencesourMCCE
(seeFig.2).
Figure1. Amultilevelapproachtobuildingamodelofemo- To understand how emotion regulation works,
tionregulation.(A)Incognitive,affective,andsocialneuro-
wemustfirsthaveanideaofhowemotionsaregen-
scienceresearch,weseektodescribephenomenaintermsof
erated. As such, our model has two main parts—
relationships among three levels of analysis: experience and
behavior, psychological processes, and neural systems. The descriptions of the mechanisms supporting emo-
bidirectionalarrowsbetweenlevelsindicatethattherelation- tion generation on the one hand and the mecha-
shipsamongthemarebidirectional.(B)Throughmeasurement nismssupportingemotionregulationontheother.
and/orexperimentalmanipulation,neuroimagingresearchon
For the sake of simplicity, we present the psycho-
emotionregulationcanobservephenomenaatthebehavioral
logical and neural systems involved in the gener-
levelandtheneurallevelandusetheseobservationstoinferthe
natureoftheinterveningcognitiveand/oraffectiveprocesses. ation and regulation of emotion as being distinct,
The direction of the arrows from the behavioral and neural yetitshouldbenotedthatthereisevidencetosug-
levelstowardtheprocesslevelindicatesthedirectionofcausal gest that the underlying psychological14 and neu-
inference(i.e.,wecan’tobservetheoperationoftheseprocesses ral mechanisms15,16 are at least partially overlap-
directly,butinfertheiroperationbasedonbehavioralandneural
ping. Indeed, elsewhere we have noted that the
observations).
distinction between emotion generation and reg-
brainbasesofemotionregulationaswellasbeap- ulation is blurry at best (e.g., Ref. 16), and which
pliedtoaccountforotherrelatedphenomena,such term one uses may reflect their usefulness for ad-
asaffectivelearning,affect-baseddecisionmaking, dressingaparticularquestionmorethanhardand
and affective expectancies. Throughout these first fastdifferencesintheirmechanisms.Here,wetreat
twosectionswefocusprimarilyononestrategyin them separately to make points about the ways in
particular—known as reappraisal—because it has whichputativecontrolandaffect-triggeringsystems
receivedthebulkofempiricalattention.Inthethird interact.
andlastsection,wesummarizeandconsiderdirec-
Mechanismsofemotiongeneration
tionsforfuturebasicandtranslationalresearch.
Ouraccountofhowemotionsaregeneratedismul-
Amodelofthecognitivecontrolofemotion
tileveled12 in its description of both the processes
Any model of emotion regulation (or any other and the neural systems that give rise to emotional
phenomenon)ispredicatedonassumptionsabout responses.
howdifferentlevelsofanalysisfittogether.Ouras-
sumptionsfollowthosenowcommonplaceincog- Processesinvolvedingeneratingemotion
nitive, affective, and social neuroscience in which TheblacktimelineatthebottomofFigure2Ashows
researchers seek to describe phenomena in terms asimplemodeloffourstepsinvolvedingenerating
oftherelationshipsamongthreelevelsofanalysis: emotional responses.17 In the first step, a stimu-
behavior/experience, process, and neural systems lus is perceived in its current situational context.
(Refs. 11–13; Fig. 1A). Neuroimaging research on The stimulus could be an internal thought, feel-
emotionanditsregulationcanobservephenomena ing, or sensation, or any number of external cues,
atthebehaviorallevel(e.g.,measuresofemotional ranging from a facial expression or gesture to an
response and the specific regulatory strategies one action or event. At the second stage, one attends
mightemploy)andtheneurallevel(e.g.,fMRImea- to some of these stimuli or their attributes.What-
suresofbrainactivity)andusetheseobservationsto ever is in the focus of attention is passed along
inferthenatureoftheinterveningcognitiveand/or to subsequent emotion generative stages, whereas
affectiveprocesses(Fig.1B). ignored or unattended stimuli may be either
E2 Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences.
Ochsneretal. Functionalimagingstudiesofemotionregulation
Figure2. Amodelofthecognitivecontrolofemotion(MCCE).(A)Diagramoftheprocessingstepsinvolvedingeneratingan
emotionandthewaysinwhichcognitivecontrolprocesses(bluebox)mightbeusedtoregulatethem.Asdescribedinthetext,
theeffectsofdifferentemotionregulationstrategies(theredarrowsdescendingfromthecognitivecontrolprocessesbox)canbe
understoodintermsofthestagesoftheemotiongenerationsequencethattheyinfluence.Thepinkboxseenattheappraisalstage
ismeanttoindicatethatneuralsystemsinvolvedingeneratingemotionsupportthisprocess.(B)Neuralsystemsinvolvedinusing
cognitivestrategies,suchasreappraisal,toregulateemotion(left,blueboxes),systemsinvolvedingeneratingthoseresponses(left,
pinkboxes),andsystemswithanundefinedorintermediaryroleinreappraisal(left,yellowboxes).
excluded from these stages or receive diminished strategiescanaffectchangesinsomeorallofthem,
subsequentprocessing.Thethirdstageinvolvesap- dependingonthestrategy.
praisingthesignificanceofstimuliintermsoftheir
relevance to one’s current goals, wants, or needs. Neuralsystemsinvolvedingenerating
This is the stage focused on by appraisal theories emotion
of emotion, which describe the structure of dif- Reviews and meta-analyses of functional imaging
ferent appraisals that lead to positive versus neg- studies19,20 indicate that a number of cortical and
ative reactions in general and to specific types of subcorticalbrainsystemsmayplaykeyrolesinthe
emotional responses in particular.18 Because the appraisaland/orresponsestagesofemotiongener-
current neuroscience literature suggests that there ation. For present purposes, we focus on the four
maynotbespecificneuralsystemsfordifferentdis- thathavebeenmostfrequentlydiscussedinstudies
creteemotions,19,20forpresentpurposes,wesimply ofreappraisalinparticular,andemotionregulation
distinguish between basic positive/appetitive ver- strategiesmoregenerally(seeFig.2B;forexamples
sus negative/aversive appraisals that have been re- ofotheremotionsystemsthatmaybemodulatedby
liably associated with specific neural systems that emotionregulation,seeRefs.9and22).
are described below. Finally, the fourth stage in- Thefirstistheamygdala,whichisinvolvedinthe
volves translating these appraisals into changes in perceptionandencodingofstimulirelevanttocur-
experience, emotion-expressive behavior, and au- rentorchronicaffectivegoals,23,24rangingfromre-
tonomic physiology. Although these three indica- wardsorpunishmentstofacialexpressionsofemo-
torsofemotionalresponsedonotalwayscorrelate tion to aversive or pleasant images and films.25–27
withoneanotherforreasonsthatarenotperfectly Although the amygdala generally is sensitive to
understood,21 as noted below, emotion regulation detecting and triggering responses to arousing
Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences. E3
Functionalimagingstudiesofemotionregulation Ochsneretal.
stimuli,28itexhibitsabiastowarddetectingcuessig- responses through the active engagement of regu-
nalingpotentialthreats,likeexpressionsoffear.29–31 latory processes. That said, we can further distin-
The second is the ventral striatum, which is in- guish between cases where emotion regulation is
volved in learning which cues (ranging from so- guidedbyregulatorygoalsthatareimplicitorout-
cial signals, like smiling faces, to actions, to ab- sideawareness(e.g.,Ref.57)ascomparedwithex-
stract objects) predict rewarding or reinforcing plicit and accessible to awareness. Although both
outcomes.32–34 areinterestingandimportant,noneurosciencere-
The third is the ventromedial prefrontal cortex search has addressed the former case and a great
(vmPFC), which integrates affective valuations of dealhasaddressedthelattercase.Therefore,wefo-
specific stimuli made by the amygdala and ventral cushereonthedeliberatedeploymentofanemotion
striatumwithinputsfromotherregions,including regulationstrategyintheserviceofexplicitgoalsto
medial temporal lobe systems that provide histor- changeone’semotions.Tounderstandhowsuchex-
ical information about prior encounters with the plicitemotionregulationstrategieswork,itisuseful
stimuli as well as inputs from brainstem motiva- todistinguishamongfiveclassesofstrategieswhose
tional and prefrontal control centers that provide effects on emotion can be understood in terms of
informationaboutcurrentbehavioralgoals.35–43As the stage of the emotion generation sequence on
such, vmPFC tracks the positive or negative valu- whichtheyhaveanimpact.58
ation of stimuli in a context and goal-dependent Itisimportanttonotethatthedistinctionsmade
manner.41,44–46Examplesofthisincludethefinding below originally were based on behavioral analy-
thatvmPFCactivitytoanimageofahealthybutnot ses of the aspects of emotional responses targeted
tastyfooddependsonwhetheronehasthegoalto by different strategies.58 As such, this analysis was
eathealthily,47andthefindingsthatvmPFClesions agnostic to the specific nature of the regulatory
leadtocontext-inappropriateaffectiveresponsesin processes supporting each strategy, but tacitly as-
bothhumansandanimals.39,48,49 sumed that all strategies drew upon some combi-
The fourth brain system is the insula, which is nation of cognitive control processes (designated
thoughttorepresentaviscerotopicmapofascend- by the blue box in Fig. 2A). In this regard, func-
ingviscerosensoryinputsfromthebody50 andhas tionalimaginghasmadeasubstantialcontribution
beenimplicatedinnegativeaffectiveexperiencein to our understanding of how emotion regulation
general.51,52Thereappearstobeposterior–anterior works because it provides insight into the nature
functionalgradientintheinsulawithposteriorre- ofthecontrolprocessessupportingemotionregu-
gions associated with primary representations of lation that is not obtainable from behavioral data
sensationsfromthebodyandanteriorregionsasso- alone.9
ciatedwithinteroceptiveawarenessofthebodyand As illustrated by the top portion of Figure 2A,
inmotivationalandaffectivestates,likedisgust,that thefirsttwostrategiesinvolvechangingthenature
haveastrongvisceralcomponent.51,53–56 of the stimulus inputs to the emotion generation
cycle.Insituationselection,youkeepyourselfaway
Mechanismsofemotionregulation fromstimulithatelicitunwantedemotionsandput
yourselfinthepresenceofstimulithatelicitdesired
Withanunderstandingofhowemotionsaregener-
emotions.Anexampleisstayingawayfromaparty
atedinthefirstplace,wecanturntoanaccountof
whereanoldflamewillbepresentifyoudon’twant
theprocessesandneuralsystemsinvolvedinregu-
tofeelpangsofsadnessforhavingbeendumpedby
latingthem.
her.Situationmodificationiswhenyoufindyourself
Processesinvolvedinemotionregulation inthepresenceofastimulusthatelicitsanunwanted
Althoughmanybehaviorscanchangeouremotions, emotionandchangesomethingaboutthesituation
oftentheseeffectsareunintendedorincidental(e.g., toalteritsimpactonyou.Intheoldflameexample,
your mood improves because you happen to have youmightleaveapartyatwhichsheisunexpectedly
lunchwithafriend)andassucharenotconsidered present or leave the room in which she is having
to be examples of emotion regulation, per se. In- a conversation. Although these two strategies are
stead, emotion regulation entails the modification undoubtedly effective (e.g., Ref. 59), they can be
of ongoing—or the initiation of new—emotional difficult to study neurally and have received little
E4 Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences.
Ochsneretal. Functionalimagingstudiesofemotionregulation
attention in imaging or using other neuroscience havelong-lastingeffectsonone’stendencytohave
techniques(seebelow). anemotionalresponsetoastimulus,65 presumably
Theremainingthreestrategiesareallamenableto, because only reappraisal involves an active change
andhavebeenstudied,usingimaging,albeittovary- inhowonerepresentstheaffectivemeaningofthat
ing degrees. Attentional deployment controls what stimulus.
stimuliaregatedinto,oroutof,theemotiongen-
Neuralsystemsinvolvedinemotionregulation
eration process. The two most commonly studied
As foreshadowed previously, the use of functional
exemplars10 are selective attention, which involves
imaginghasprovidedinsightintothenatureofthe
shiftingthefocusofattentiontowardorawayfrom
control systems that support regulatory strategies
stimuli or their attributes, and distraction, which
as well as the affect systems that these strategies
involves limiting attention to an external stimulus
modulate to change an emotional response. This
by focusing internally on information maintained
sectiondiscussescoreconclusionsthatcanbedrawn
inworkingmemory.Thesetypesofstrategiesdiffer
from reappraisal studies and a model of emotion
fromsituationselectioninthattheydonotinvolve
regulationthatcanbederivedfromit.
physically altering one’s proximity or relationship
to an emotional stimulus, but rather they manip-
Reappraisalasaparadigmcase. Reappraisalisan
ulate attention so as to alter one’s emotional re-
appropriatestartingpointfordevelopingaMCCE
sponse.Cognitivechangeinvolveschangingtheway
forthreereasons.First,becausereappraisalisamong
one appraises the meaning of a stimulus. It is one
themostcognitivelycomplexstrategies,amodelof
of the most cognitively complex strategies insofar
emotion regulation derived from reappraisal work
asitdrawsonanyofanumberofdifferenthigher
maybegenerallyapplicabletootherstrategiesand
cognitiveprocessestosupportchangesinstimulus
phenomena that typically will be cognitively sim-
meaning, including languageandmemory, aswell
pler. Second, the majority of studies to date have
processesthatalsosupportotherstrategies,suchas
focusedonreappraisalbecause(i)itcanbestudied
attention and response selection. The most com-
easilyinanimagingenvironmentand(ii)because
monly studied exemplar is reappraisal, which in-
itisthe strategyreferencedbycountlessaphorisms
volvesreinterpretingthemeaningofastimulus,in- thatadviseus,“[to]lookonthebrightside...”,“[to]
cluding one’s personal connection to it, to change turnasow’searintoasilkpurse...”,“Whenlifegives
one’s emotional response. Finally, response modu-
you lemons, make lemonade,” and, “[that] every
lation strategies target the systems for emotion-
dark cloud has a silver lining.” Third, in contrast
expressive behavior. The most commonly studied
to other areas of emotion regulation research (re-
exemplarisexpressivesuppression,60 whichentails
viewedbelow)reappraisalstudiestendtobemore
keepingone’sfacestillsothatobserverswouldnot
methodologically and conceptually similar to one
knowtheemotionyouareexperiencing.
another and therefore provide a stronger base for
Agreatdealofbehavioralandpsychophysiolog-
mechanistic inferences. With these considerations
ical research has been devoted to comparing and
inmind,wenowdescribefivekeyinsightsintothe
contrastingthebehavioralconsequencesofdeploy-
brain mechanisms supporting emotion regulation
ingeachofthesestrategies.Forexample,it’sknown thathavebeenderivedfromstudiesofreappraisal.9
that attentional deployment and reappraisal can
havedownstreameffectsonvariouscomponentsof Basiccontrolsystem–affectsystemrelationships.
anemotionalresponsebecausetheytargettheearly WhenthefirstfMRIstudiesofreappraisalwerepub-
stagesoftheemotiongenerationsequence.60–65 By lished approximately 10 years ago, there were no
contrast, expressive suppression has an impact on imagingstudiesofanyformofemotionregulation.
only the behaviors it targets at the final response Todevelophypothesesabouthowreappraisalmight
stageofemotiongeneration;whenkeepingyourface work,ananalogywasdrawnbetweentheuseofcog-
still,emotionalexperiencemaysubtlydiminish,66,67 nitiontocontrolemotionandtheuseofcognition
ifatall,andyourphysiologicalarousalwillincrease to control memory, attention, and other thought
fromtheeffort.60Thereisalsoevidencethatstrate- processes.43Thesimpleideawasthatprefrontaland
gies differ in their long-term effects. For example, cingulatesystemswouldsupportcontrolprocesses
reappraisal,butnotdistraction,hasbeenshownto thatmodulateactivityinposteriorandsubcortical
Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences. E5
Functionalimagingstudiesofemotionregulation Ochsneretal.
systems that generate emotional responses.10 A tactics (panel B), and the valence of the emotion
decadeandover50imagingstudieslater,thisinitial being regulated (panel C). Ignoring these distinc-
hypothesishasbeenstronglysupported. tions for a moment, one can see that the control
Figure2Bschematicallyillustratesthebrainsys- system–affectsystemrelationshipsshowninFigure
tems shown by current research to be involved in 2Banddescribedpreviouslyhavebeenobservedre-
thecognitivecontrolofemotionviareappraisal.As liablyacrossnumerousstudies.
such, Figure 2B diagrams the core elements of the
Movingbeyondthebasicmodel
MCCE.Threetypesofneuralsystemsareprimarily
involvedingeneratingandapplyingreappraisals.10 Withtheconsistencyofthecorecontrol–affectsys-
First, dorsolateral and posterior prefrontal cor- tem relationship as a foundation, we are now in
tex, along with inferior parietal regions gener- a position to consider how this basic model—first
ally implicated in selective attention and working proposedin200243 andelaboratedin200510—has
memory, may be used to direct attention to evolved.Belowwediscussfirstnewconclusionsthat
reappraisal-relevant stimulus features and hold in canbedrawnaboutthemodelfromrecentstudiesof
mind reappraisal goals as well as the content of reappraisal.Inthissection,wepayspecialattention
one’s reappraisal.68–70 Second, dorsal regions of totwoemergingfeaturesofthemodel:(i)thepo-
the anterior cingulate cortex implicated in perfor- tentialintermediaryroleofsemantic/perceptualsys-
mance monitoring may help track the extent to temsinreappraisal,and(ii)pathwayslinkingcon-
whichone’scurrentreappraisalsarechangingemo- trolandaffectsystems.Next,wediscussthewayin
tional responses in the intended way.71 Third, re- which the model can be applied to understanding
gions of ventrolateral prefrontal cortex implicated regulatorystrategiesotherthanreappraisalaswellas
in selecting goal-appropriate (and inhibiting goal- various allied phenomena involving control–affect
inappropriate)responsesandinformationfromse- systeminteractions.
mantic memory may be used to deliberately se-
lectanewstimulus-appropriatereappraisalinfavor Integratingnewresearchonreappraisal
of one’s initial prepotent appraisal of that stimu-
Recentresearchprovidesnewinsightintothedistri-
lus.72,73 Finally,totheextentthatone’sreappraisal
butionofemotionregulation–relatedactivationfoci
involves focusing on and interpreting or reinter-
asafunctionofreappraisalgoals(i.e.,theoutcome
preting one’s own emotional states—or those of
one hopes to achieve by regulating, for example,
others—dorsomedialprefrontalregionsimplicated
increasingordecreasinganemotionalexperience),
inattributingmentalstatesalsomaybeactive.74,75
tactics(i.e.,thespecificsubtypeofreappraisalone
Withrespecttotheemotion-relatedregionsthat
implements), and the emotional valence of stim-
aremodulatedbyreappraisal,thefourregionsde-
uli (i.e., whether the stimulus evokes a positive or
scribed earlier in the section on neural systems
negativeemotionalresponse).Here,weconsiderthe
foremotiongenerationallhavebeenimplicated—
implicationsofthisworkfortheevolvingMCCE.
albeit to differing extents. Far and away, the most
commonly modulated region is the amygdala, fol- Goalspecificity
lowed by the ventral striatum. The insula and the Arguably,themostcommongoalwhenusingreap-
vmPFC are the least commonly modulated re- praisalistodecreasenegativeemotion,aswhenwe
gions9,10(althoughseethesectiononpathwaysbe- attempt to make ourselves feel better about a dis-
lowforapotentialroleofvmPFCinreappraisalas appointing paper rejection, an argument, and the
amodulator). like.Itisnotsurprisingthenthatthisgoalhasbeen
Although we will discuss the significance of the thefocusofthemajorityofreappraisalstudies(see
differential modulation of these regions in more Table1).Thisisnottheonlygoalthatguidesreap-
detail later (see later sections on valence speci- praisal,however.Insomecases,aswhenweworry,
ficityandpathways),fornowwecanhighlightthe ruminate,ormakeourselvesmoreanxiousorfearful
consistency with which they have been observed. byelaboratingonthemeaningofunpleasantevents,
Figure 3 plots peak activation foci for 43 studies weareusingreappraisalinserviceofthegoaltoin-
(seeTable1)ofreappraisalinhealthyindividualsas crease emotion. A small, but growing, number of
afunctionofreappraisalgoals(panelA),reappraisal studieshaveexaminedthisreappraisalgoalaswell.
E6 Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences.
Ochsneretal. Functionalimagingstudiesofemotionregulation
Figure 3. Plotsofactivationfocifromthe43studiesofreappraisaldescribedinthetextandTable1.(A)Plotsoffociasa
functionofthegoalstodecreaseorincreaseemotion.(B)Plotsoffociasafunctionofthespecificreappraisaltacticsused—either
reinterpretingthemeaningofeventsdepictedinstimulioractivelychangingone’spsychologicaldistancefromthem.(C)Plotsof
fociasafunctionofthevalenceofthestimulielicitingtheemotionsthatparticipantsattemptedtoregulate.Blueboxesillustrate
regionsthatarepurportedtosupportreappraisal(increase>lookanddecrease>lookcontrasts).Pinkboxesillustrateregions
thatarepurportedtobemodulatedbyreappraisal(look>decreaseandincrease>lookcontrasts;forclarity,onlyfocifalling
withintheboundariesoftheamygdalaandstriatumareshown).
Figure 3A plots peak activation foci for reap- Second, there is some evidence that increase
praisal studies of healthy individuals as a function goals differentially involve anterior portions of
ofdecreaseversusincreasegoals.Perusalofthisfig- dorsomedial prefrontal cortex (dmPFC). Of the
ure highlights three findings. First, whereas both 12 studies directly comparing increasing emotion
increase and decrease goals recruit left prefrontal with a control condition in which participants
regions, decrease goals recruit right prefrontal re- respond naturally, six show increases in anterior
gions to a much greater extent than do increase dmPFC.16,76,81–83 Of the six studies that did not,
goals.Therearetwointerpretationsofthisfinding. mostshowedactivationinneighboringareas(such
First,itmaybeattributabletothefactthatdecreas- as anterior cingulate cortex).62,84–88 Given the role
inganemotionalresponseismoredifficultthanin- of dmPFC in making judgments about mental
creasingone,andthereforemayrequireadditional states75,89,90 and that the majority of reappraisal
cognitivecontrolresources.76Second,decreasing— studies use photographs of people as stimuli (see
butnotincreasing—anemotionalresponserequires Table 1), it is likely that these regions support
inhibitingorlimitingtheexpressionofaprepotent attentiontoandelaborationofemotionalstates,in-
appraisalofastimulus(e.g.,asnegative)infavorof tentions,andoutcomesoftheindividualsdepicted
selectinganalternativereappraisal(e.g.,asneutral inthesephotos.
orevenpositive).Researchshowsthatrightdorsal— Third,whereasincreaseanddecreasegoalsboth
andespeciallyventrolateral—prefrontalcortexisin- seemtomodulatethestriatum(includingboththe
volvedintheselectionand/orinhibitionofvarious caudateand putamen), theymay differin the way
kindsofresponses.77–80 they modulate the amygdala. On the one hand,
Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences. E7
Functionalimagingstudiesofemotionregulation Ochsneretal.
Table1.Neuroimagingstudiesofreappraisalinhealthyindividualsa
Design
Stimulus Timingof
Study Participants Goal Valence Tactic type reappcue Amygdala
Beauregardetal.204 HYA Dec Pos Dist Videos Early∗ No
Domesetal.81 HYA Both Neg Both Photos Late Yes
Eippertetal.84 HYA Both Neg Both Photos Late Yes
Erketal.168 HC Dec Neg Dist Photos Early Yes
Goldinetal.66 HYA Dec Neg Reint Videos Early Yes
Harenskietal.205 HYA Dec Neg Both Photos Early Yes
Hayesetal.139 HYA Dec Neg Reint Photos Late Yes
Herwigetal.206 HYA Dec Both Reint Anticipate Early Yes
photos
Hollmannetal.207 HYA Dec Pos(food) Reint Photos Early No
Ichikawaetal.82 HYA Both Neg Reint Task Early∗ No
(errors) errors
Kanskeetal.127 HYA Dec Both Both Photos Late Yes
Kimetal.95 HYA Dec Both Reint Photos Early Incpos
only
Koberetal.118 HYA Dec Pos Reint Photos Early Yes
smokers (food/cigs)
andnon-
smokers
Koenigsburgetal.199 HYA Dec Neg Dist Photos Early Yes
Krendletal.208 HYA Dec Neg Unclear Photos Early Yes
Krossetal.112 HYA Dec Neg Reint Memories Late No
Langetal.83 HC Both Neg Dist Scripts Early Inconly
Levesqueetal.209 HYA Dec Neg Dist Videos Early∗ No
Maketal.210 HYA Dec Both Unclear Photos Early∗ No
McRaeetal.211 HYA Dec Neg Reint Photos Early Yes
McRaeetal.61 HYA Dec Neg Reint Photos Early Yes
McRaeetal.180 Healthyaged Dec Neg Reint Photos Early No
10–22
McRaeetal.15 HYA Dec Neg Reint Photosof Early Yes
faces
Modinosetal.212 HYA Dec Neg Reint Photos Late Yes
Newetal.85 HC Both Neg Reint Photos Late Yes
Ochsneretal.43 HYA Dec Neg Reint Photos Late Yes
Ochsneretal.76 HYA Both Neg Both Photos Early Yes
Ochnseretal.16 HYA Inc Neg Both Photos Early Yes
Ohiraetal.115 HYA Dec Both Unclear Photos Early∗ Yes
Opitzetal.96 HYAand Both Neg Reint Photos Late No
HOA
Phanetal.114 HYA Dec Neg Reint Photos Early∗ Yes
Pitskeletal.86 Healthyaged Both Neg Reint Photos Early Yes
7–17
Continued
E8 Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences.
Ochsneretal. Functionalimagingstudiesofemotionregulation
Table1.Continued
Design
Stimulus Timingof
Study Participants Goal Valence Tactic type reappcue Amygdala
Schardtetal.213 HYA Dec Neg Dist Photos Early Yes
Schulzeetal.87 HC Both Neg Both Photos Late No
Staudingeretal.214 HYA Dec Pos Dist Reward Early∗ No
Staudingeretal.215 HYA Dec Pos Dist Anticipate Early∗ No
reward
Urryetal.94 HOA Both Neg Reint Photos Late Inconly
Urryetal.216 HOA Both Neg Reint Photos Late Yes
vanReekumetal.88 HOA Both Neg Reint Photos Late Deconly
Vrtickaetal.217 HYA Dec Both Reint Photos Early∗ Yes
Wageretal.117 HYA Dec Neg Reint Photos Early Yes
Walteretal.218 HYA Dec Neg Dist Photos Early Yes
Winecoffetal.195 HYAand Dec Both Dist Photos Late Yes
HOA
aStudiesareorderedfirstbyyearandsecondbyalphabeticalorder.
Onlystudiesthatreportedcontrasts(i.e.,notonlyfunctionalconnectivityorcorrelationalanalyses)forpsychologically
healthyindividualsareincludedhere.Ifastudyincludedapatientsamplebutstillreportedresultsforitshealthyadult
controlsseparately,itwasincluded.
HYA,healthyyoungadults,typically18–30yrsold;HOA,healthyolderadult,typicallyaged60yearsorolder;HC,
healthyadultcontrolparticipantsmatchedtopatients;Fordesign,Goal,goalpursuedbyparticipantstoincreaseor
decreaseemotionalresponses;Valence,Positiveornegativelyvalencedemotionalstimuli;Tactic,typeofreappraisal
used,distancingorreinterpreting;StimType,stimulustype;Timingofreappcue,timingofinstructioncuetoreappraise
relativetoonsetofstimulus,whereearlyisjustbeforesimulusonsetandlateisafewsecondsafterstimulusonset;
Amygdala,whethermodulationofamygdalawasreported.
Note: All studies used event-related designs (different types of trials are presented in a randomized fashion so as
toestimateresponsesonatrial-by-trialbasis)excepttheninestudiesdesignatedby∗ inthe“Timingofreappcue”
column,whichindicatesthattheyusedablockdesign(trialsare“blocked”bytype,suchthatmanyofonetypeappear
consecutively).Also,forthestimulus-typecolumn,photostimuliweredrawnfromtheinternationalaffectivepicture
system111 unlessotherwisespecified.Goal:Dec,decrease;Inc,increase;Both,bothincreaseanddecreaseconditions
wereused;Valence:Neg,negative;Pos,positive;Both,bothpositiveandnegativestimuliwereused;Strategy:Both,
bothdistancingandreinterpretingwereused(thisonlyappliestoRef.76),orparticipantsweregiventhechoiceof
distancingorreappraising;Dist,becomemoreorlesspsychologicallydistant;Reint,cognitivelyreinterpret;Unclear,
unclearastowhattacticwasinstructed.
decrease goals reliably modulate the amygdala’s creasegoalsinfluencetheoutputsoftheamygdala,
ventral (corresponding to the basal and lateral which flow from the central nucleus.43,76 This hy-
amygdalanuclei)anddorsalportions(correspond- pothesis would fit with anatomical data showing
ingtothecentralnucleus)aswellasthesublentic- that the basolateral complex has reciprocal con-
ularextendedamygdala(SLEA30,91,92)thatliesbe- nections with ventrolateral PFC as well as tempo-
tweentheamygdalaandthestriatum.Ontheother ral and parietal regions implicated in visuospatial
hand,increasegoalsmaymodulateonlythedorsal and semantic representation, whereas the central
amygdala/SLEA. One speculative interpretation of nucleus receives inputs from medial prefrontal re-
these data is that decrease goals influence percep- gionsandsendsoutputstoautonomiccentersthat
tual and semantic inputs to the amygdala, which implement various components of an emotional
comethroughthebasolateralcomplex,whereasin- response.93
Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences. E9
Functionalimagingstudiesofemotionregulation Ochsneretal.
The major caveat for all of these conclusions, distancing,whichinvolveschangingone’spersonal
however, is that very few studies have examined connection to, or psychological distance from, the
increase goals, and as a consequence, conclusions stimulusthatelicitsemotion.Intheexampleofthe
aboutthegoalspecificityofreappraisal-relatedacti- photoofthesickman,onemightdecreaseemotion
vations must be considered tentative. That being by viewing the image from the detached perspec-
said, the first study to directly compare increase tive of an objective, third person observer and/or
and decrease goals within subjects obtained ex- imaginingthatthepicturedeventtookplacealong
actly the results described previously76—both in- time ago or in a faraway location. One might in-
creasinganddecreasingnegativeaffectrecruitedleft creaseemotionbyinsteadimaginingthatoneisex-
vlPFCanddlPFCandmodulatedthedorsalamyg- periencingpicturedeventsinthepresentmoment,
dala/SLEA(increasingaffectincreasedamygdalaac- fromafirst-personperspective,whichenablesyou
tivity,whereasdecreasingnegativeaffectdecreased to smell, hear, and directly observe what is taking
activity),yetitwasalsorevealedthatincreasingneg- place.
ativeaffectrecruitedthedmPFCtoagreaterdegree As Table 1 shows, about twice as many studies
than did decreasing negative affect and decreasing have examined reinterpretation as have examined
negativeaffectrecruitedrightvlPFCandmodulated distancing,withafewallowingparticipantstoen-
ventralamygdalatoagreaterextentthandidincreas- gageineithertactic,andonlyasinglestudydirectly
ingnegativeaffect.Atleasttwo-thirdsofsubsequent comparingthem.76 Figure3Bplotspeakactivation
studiescomparingthesegoalshaveobtainedresults foci for reappraisal studies of healthy individuals
that are generally consistent with them76,84,87,94–96 as a function of reinterpretation versus distancing
(other findings also have been reported, includ- tactics.
ingincreaseversusdecreasedifferencesonlyinthe Thisfigureillustratesthreeconclusionsthatcan
amygdala,81 striatalmodulation,76,88,94 andgreater bedrawnaboutreappraisaltactics.First,reinterpre-
right PFC activation for increasing than decreas- tationseemstodifferentiallycalluponventrallateral
ing84). prefrontalregionsimplicatedinresponseselection
and inhibition.73,98,99 Presumably, this reflects the
Tacticspecificity fact that reinterpretation requires that one must
Inthemilitary,adistinctioniscommonlymadebe- look up and select alternative meanings for stim-
tween strategy and tactics. Strategy is the overall ulifromsemanticmemorytoagreaterextentthan
means by which a goal (e.g., win the war) is to be doesdistancing.Second,distancingseemstorecruit
achieved(e.g.,divideandconquer).Tacticsarethe parietalregionsimplicatedinspatialattentionand
specificwaysinwhichstrategiesareimplementedin representation to a greater extent, including per-
agivencircumstance(e.g.,aquickinfantryadvance, spectivetakingandthesenseofagency.100–103 This
anairstrike,etc.).Inthesameway,onecandistin- mayreflectthefactthatdistancinginvolveschang-
guishbetweenreappraisalasastrategythatinvolves ingtheconceptualandspatiotemporalperspective
changingthemeaningofastimulusandthetactics fromwhichstimuliareexperienced.Third,ingen-
usedtoimplementthatstrategy.97 eral,theregionsinvolvedinreinterpretationappear
Twodifferentreappraisaltacticshavebeenstud- tobemorestronglyleftlateralizedinprefrontaland
iedwithimaging.9,76Thefirstcanbecalledreinter- temporalcortices,whereasregionsinvolvedindis-
pretation, which involves changing one’s interpre- tancing appear to be more strongly right lateral-
tation of the elements of the situation or stimulus izedinprefrontalcortex.Thesepatternsmayreflect
thatelicitsemotion.Forexample,ifoneispresented thedifferentialdependenceofreinterpretationand
withaphotoofasickmaninthehospitalthatelic- distancing on linguistic and semantic processes as
its feelings of sadness, one might reinterpret this opposedtospatialandattentionalprocesses,which
image in a way that decreases emotion by think- generallyshowaleftversusrighthemispherepattern
ingabouttheman’sheartyconstitutionandthathe ofrelativespecialization.76,104
will be healthy and well in the future. To increase Here again, however, because comparatively
emotion, one might instead think about how the fewer studies have examined distancing, firm
manisinagreatdealofpainandmay,infact,get conclusions concerning the tactic specificity
worse and even perish. The second can be called of reappraisal-related activations await further
E10 Ann.N.Y.Acad.Sci.1251(2012)E1–E24(cid:2)c 2012NewYorkAcademyofSciences.