Epilogue—The nature of emotion: A research agenda for the...

Fox/Shackman,Epilogue1

Epilogue—Thenatureofemotion:Aresearchagendaforthe21stcentury

AndrewS.Fox*

Department of Psychology and California National Primate Research Center, University of California,Davis,CAUSA

ReginaC.Lapate

DepartmentofPsychologyandHelenWillsNeuroscienceInstitute,UniversityofCalifornia,Berkeley,CAUSA

RichardJ.Davidson

CenterforHealthyMinds,UniversityofWisconsin—Madison,Madison,WIUSA

AlexanderJ.Shackman*

Department of Psychology, Neuroscience and Cognitive Science Program, andMarylandNeuroimagingCenter,UniversityofMaryland,CollegePark,MDUSA

*A.S.FandA.J.S.contributedequallytothiswork;theorderofauthorswasdeterminedbyacoinflip.

Pleaseciteas:

Fox,A.S.*,Lapate,R.C.,Davidson,R.J.&Shackman,A.J.*(inpress).Epilogue—Thenatureofemotion:Aresearchagendaforthe21stcentury.InFox,A.S.,Lapate,R.C.,Shackman,A.J.&Davidson,R.J.(Eds.).Thenatureofemotion:Fundamentalquestions(2nded.).NewYork:OxfordUniversityPress.

AddressCorrespondenceto:

AndrewS.Fox([email protected])–or–AlexanderJ.Shackman([email protected])

Fox/Shackman,Epilogue2Emotion plays a central role in human experience and there is an abiding interest, among scientists,

clinicians, and the public at large, in understanding the nature of emotion, identifying its biological

underpinnings, and determining its contribution to other psychological processes, from cognition and

decision‐making,tohealthanddisease.Overthepasttwenty‐fiveyears,methodsforeliciting,assessing,

and analyzing emotion have become increasingly refined (e.g., Coan & Allen, 2007; Dan‐Glauser &

Scherer,2011;Kramer,Guillory,&Hancock,2014;Samson,Kreibig, Soderstrom,Wade,&Gross,2015;

Soto&John,inpress)andtechniquesformakingsenseoftheunderlyingneurobiologyhavebecomemore

powerfulandprecise(e.g.,Glasseretal.,2016;Kim,Adhikari,&Deisseroth,2017;Urban&Roth,2015;

Woo, Chang, Lindquist, &Wager, 2017). The 92 essays that compriseTheNature ofEmotion embody

these exciting developments andmake plain the important conceptual advances that have beenmade

sincethepublicationofthefirsteditionin1994.Despitethisprogress,itisclearthatourunderstanding

remainsfarfromcomplete.Here,weoutlinearoadmaptothemostimportantstrategiesandavenuesfor

futureresearchintheaffectivesciences.Webeginbydiscussingtwooverarchingconceptualissuesthat

are likely to be of interest to all students of emotion. In the second section, we highlight the most

importantmethodologicalchallengesconfrontingthefieldandprovidesomespecificrecommendations

foraddressingthem.Finally,inthethirdsection,wedescribeseveralofthemostexcitingandpotentially

fruitfulspecificavenuesforfutureresearch.

OVERARCHINGCONCEPTUALISSUES

In this section, we describe two overarching conceptual issues: first, the need to develop a deeper

understandingoftheprocesseslinkingemotionalantecedentstotheirresponsesand,second,thevalue

andproperplaceofneurobiologyinthestudyofemotion.Webelievethatbothoftheseissueshavefar‐

reachingimplicationsforallstudentsofemotion.

Fox/Shackman,Epilogue3UnderstandingtheLinksConnectingEmotionalStimuliandResponses

Oncedetected,emotionstimulicansparkarangeofresponses,includingthoughts,behaviors,peripheral

physiological changes, and, of course, feelings. Most of the contributors agree that emotions are

functional,andinvolvethiskindofcomplex,multi‐componentialresponse(Question1),butthereisno

clear consensus on how emotional inputs—including foreground cues (e.g., predator), contextual cues

(e.g., escape route), and interoceptive cues (e.g., fatigue)—are evaluated and used to select the most

adaptiveemotionalresponse(Blanchard&Pearson,thisvolume;Moaz&Bar‐Haim,thisvolume;Averill,

1983;Clore,1994;Ekman,1977,1994b;Ekman&Cordaro,2011;Ekman&Friesen,1975;Frijda,1994a,

1994b, 1994c; Lazarus, 1991, 1994a, 1994b; LeDoux, 1994, 2014; Levenson, 2011), although some

valuablecluesarejustbeginningtoemerge(e.g.,Fadoketal.,2017).Inshort,westilldonothavesolid

answerstoquestionssuchas,Howdoestheorganismdeterminethemostappropriatefeeling(e.g.,anger

vs.fear),titratetheintensityoftheresponse(e.g.,mutteringunderone’sbreathvs.overtphysicalviolence),

and selectanappropriate suiteof somatomotor responses (e.g., flightvs.defensiveattack)?Howdoesan

individual “know” (i.e.,predict)which response ismostadaptive?Howdo these selectionprocessesdiffer

acrossemotions,antecedents,andcontexts?

Themostinfluentialcontemporarytheoriesofemotionincludebasicemotionmodels(e.g.,Panksepp,this

volume; Ekman & Cordaro, 2011), appraisal models (Ellsworth, this volume; Scherer, Schorr, &

Johnstone, 2001), and constructivist models (e.g., Barrett, this volume). Each suggests a different

mechanismbywhichemotionscometobeand,althoughno theoryhasclearlyemergedasa “winner,”

eachapproachhasprovedusefulinitsownright.Basicemotionmodelshaveprovidedaframeworkfor

cross‐culturalandcross‐speciesstudiesofemotionsandhelpedtoorganizethefield.Thebasicemotions

model argues that emotions stem from an automatic appraisal process of distinct and universal

Fox/Shackman,Epilogue4antecedent events. Appraisal models, which have guided our understanding of emotion regulation,

propose a substantial and elaborate appraisal process thatdynamicallyunfolds over time and suggest

that intermediate cognitions lead to an emotional response. Finally, constructivist models, posit that

every emotional experience is different; that emotions are social constructs rather thannatural kinds.

Theyaimtoexplainthevarietyofemotionalexperiencesbyinvokingprinciplesofprediction—emotions

aresaidtoexisttomakemeaningof incomingsensationsandfundamentallydependonanindividual’s

conceptualrepresentationsoftheworld.Althoughthebasicemotionsmodelandtheconstructivistmodel

are often pitted against each other, most of the contributors to The Nature of Emotion seem to

acknowledge and, more importantly, make use of both perspectives. For example, Lee & Anderson

suggestthat“Basicexpressionsmaynotbestronguniversalcategoriesbuttheevidencefortheirfunctional

origins provides a parsimonious, empirical account of their cultural consistency.… it is likely that these

adaptive action tendencies were socially co‐opted for communication, serving as anchoring sources of

invarianceinexpressionperceptionacrossculturesandcontexts”(Lee&Anderson,thisvolume).Likewise,

Freeman proposes a dynamicmodel of emotion perception that links basic‐emotion‐like (bottom‐up)

cueswith constructivist‐like (top‐down) influences that interact and stabilize onto particular percepts

overtime(Freeman,thisvolume).

Akeychallengeforthefieldwillbetodevelopnewtheoriesthatexplainhowemotionscometobe.There

isclearneedfortestable,biologicallyplausiblehypothesesthataddressthecomplexmappingbetween

emotionalantecedentsandtheirconsequents.Wehopethat inthenexteditionthetimewillberipeto

ask,“Howareemotionalstimulilinkedtoemotionalresponses?”

TheConceptualValueofNeuroscience

Fox/Shackman,Epilogue5OneofthemoststrikingdevelopmentssincetheinitialpublicationofTheNatureofEmotion(1994)has

beenthegrowingprominenceofneuroscientificapproaches toemotionorwhathasbecomepopularly

knownasaffectiveneuroscience (R. J.Davidson&Sutton,1995;Panksepp,1992,1998).Butwhatisthe

addedvalueofstudyingthebrainforunderstandingemotion?Canaffectiveneurosciencereallyprovide

theoretical insights that go beyond the reach of more traditional measures—behavior, ratings, and

peripheralphysiology(Bradley,2000;Bradley&Lang,2000,2007)?Thisisnotanabstractorrhetorical

question.Skepticshavequestionedwhetherneurosciencecanprovideconceptuallyimportantevidence

oradjudicatebetweenalternativetheoreticalmodels(e.g.,Coltheart,2013)andhundredsofmillionsof

research dollars have been spent on the assumption that it can.Many of the essays contained in the

presentvolumesay theanswer isYes.Taken together, theyprovidecompellingevidence thatstudying

thebrainisusefulfordeterminingthenature,andnotjustthebiologicalbases,ofemotion.

Neurobiologyhasproven tobeparticularlyhelpful forunveilingotherwisehidden featuresofemotion

(Questions 4 and 5; see also Adolphs, 2017). Neurobiological evidence teaches us, for example, that

reward (orpleasure) isnota single, indivisible thing,but can insteadbe split intowanting (appetitive

motivation, craving, and desire) and liking (hedonic pleasure and positive affect). Under normal

conditions, wanting and liking are exceedingly difficult to tease apart using behavioral or self‐report

methods(Havermans,2011).Thischallengereflects the fact thatwantingand likingareusually tightly

coupled:humansandotheranimalsaremotivatedtoworkharderforthingsthatweenjoymore(e.g.,an

expertlyprepared,gourmetdishvs.lukewarmporridge)andthisappetitivedriverapidlydeclinesonce

ourdesiresaresated.Yet,twodecadesofcarefulstudyprovidescompellingevidencethatwantingand

liking reflect the operation of dissociable neural systems (Berridge & Kringelbach, 2015; Berridge &

Robinson,2016;Kringelbach&Berridge,2012).Wantingcriticallydependsondopaminergicprojections

coursing from the brainstem to the nucleus accumbens,whereas liking reflects tiny ‘hotspots’ nestled

Fox/Shackman,Epilogue6withintheaccumbensandneighboringregionsof theventralstriatum. Inrodents,stimulationof these

hedonic hotspots with opioids or cannabinoids—the endogenous neurochemicals underlying the

pleasures of heroin and marijuana—selectively amplifies facial expressions of liking without altering

wanting (i.e., willingness to work for reward). A similar story has emerged for fear, with mounting

evidence that fear can be fractionated on neurobiological grounds into two or even threemore basic

constituents, looselytermedpanic, fear,andanxiety(althoughseethesectiononnomenclature,below)

(Adolphs, 2017; Davis, Walker, Miles, & Grillon, 2010; Shackman & Fox, 2016b). Beyond their

implications for emotion theory (e.g., How many emotions are there? Are emotions organized into

families?), these data have provided new insights into both the phenomenology and mechanistic

underpinningsofsubstanceabuseandanxietydisorders.

WeencouragereaderstoreflectonthevalueofneuroscienceastheyperuseTheNatureofEmotion.We

urge the curious and the skeptical alike to read the responses to Questions 4 and 5 of this volume.

Neuroscience generally does not provide easy answers: neurons in the same region often do entirely

different things, the same neurons can be involved in entirely different processes depending on the

context,andinformationisoftenstoredacrosscomplexnetworksofneuronsdistributedthroughoutthe

brain (e.g., Berridge&Kringelbach, 2015; Fadok et al., 2017; Faull& Pattinson, 2017; Gungor&Paré,

2016;Janak&Tye,2015;Namburi,Al‐Hasani,Calhoon,Bruchas,&Tye,2016;Pearson,Watson,&Platt,

2014;Pessoa,2017;Reynolds&Berridge,2008;Sennetal.,2014;Shackman&Fox,2016a;Tovoteetal.,

2016;Xiuetal.,2014).Nevertheless,importantprogresshasalreadybeenmade.Affectiveneuroscience

has revealeddissociable circuits—enablingusparseemotions into theirmoreelementary constituents

(e.g. likingvs.wanting, describedabove) and identifieddeep similarities between seeminglydisparate

psychological constructs, including emotion, pain, and cognition (Cavanagh & Shackman, 2015; de la

Vega,Chang,Banich,Wager,&Yarkoni,2016;Pessoa,2017;Shackman,Salomons,etal.,2011).


Although neuroscience holds great promise for our understanding of emotion, neuroscience is not

sufficienttogain insight intothenatureofemotion.“Withoutwell‐characterizedbehaviorandtheories

thatcanactasaconstraintoncircuit‐levelinferences,brainsandbehaviorwillbeliketwoshipspassing

inthenight”(Krakauer,Ghazanfar,Gomez‐Marin,MacIver,&Poeppel,2017,p.484).Ourbiologycanonly

beasstrongasourbehavioralmodelsandassays.Thisneedforscientificcross‐talkisevenmorecrucial

when it comes tounderstanding the rootsofemotional traitsandemotionaldisorders, constructs that

reflect bidirectional interactions between the brain and different kinds of psychosocial experiences,

includingparentingpractices,socialsupport,maritalconflict,andsocioeconomicadversity(Crameretal.,

2012a, 2012b; Kendler, 2012a, 2012b; Kendler & Halberstadt, 2013; Schwartz, Lilienfeld, Meca, &

Sauvigné, 2016; Shackman, Tromp, et al., 2016; Zhang&Meaney, 2010). In short, scientistswho view

emotion through the lens of the neurobiology have much to learn from their non‐neuroscientist

colleagues.Likewise,studentsofemotionwhodonotthemselves“doneuroscience”havemuchtogainby

attendingtothediscoveriesofaffectiveneuroscience.

METHODOLOGICALISSUESANDRECOMMENDATIONS

In this section,we discuss some of themost importantmethodological challenges facing the affective

sciences,andprovidesomerecommendationsforaddressingthem.Ourhopeisthattheseguidelineswill

proveusefultobothproducersofaffectivescience—thosechargedwithdesigning,executing,analyzing,

interpreting, anddisseminating research—aswell as consumers and gatekeepers, including reviewers,

editors, and funders.Wider adoption of these best practiceswould enhance the credibility, inferential

utility,andpracticalsignificanceofemotionresearch.


OpenandReproducibleAffectiveScience

Understandingthenatureofemotiondemandsreproducibleresearch.Yet, theactualreproducibilityof

publishedresearchinthesocialandbiomedicalsciencesisalarminglylow(Baker,2016;Engber,2017;

Motyletal.,2017;L.D.Nelson,Simmons,&Simonsohn, inpress;Nuzzo,2015;Palmers,2016;Shrout&

Rodgers,inpress;Spellman,2015;Tackettetal.,inpress;Yong,2016)(butcf.Gilbert,King,Pettigrew,&

Wilson,2016).Theresulting‘replicationcrisis’providesacriticalopportunityformethodologicalreform

and we would be remiss if we did not highlight a few of the most important recommendations and

implications for emotion researchers (for detailed reviews, see Chambers, 2017; Munafò et al., 2017;

Nicholsetal.,2017).

DesigningEmotionResearch:Pre‐RegistrationandPower.AddressingtheCalTechgraduatingclass

of1974,theNobellaureatephysicistRichardFeynmanfamouslywarnedthat:

“Youmustnotfoolyourself—andyouaretheeasiestpersontofool…Ifyou’vemadeupyourmindtotesta

theory,oryouwanttoexplainsomeidea,youshouldalwaysdecidetopublishitwhicheverwayitcomesout.

Ifweonlypublishresultsofacertainkind,wecanmake theargument lookgood. [But]Wemustpublish

bothkindsofresult”(Feynman,1974,p.12).

Studypre‐registrationisahighlyeffectivemeansofaddressingFeynman’sconcern(Munafòetal.,2017).

Thepre‐registrationofbasicstudyelements—generaldesignandsamplingplan,analyticapproach,key

Fox/Shackman,Epilogue9outcomesandpredictions—isa‘broadspectrumtreatment’thatinoculatesagainstbothcognitivebiases

(e.g., confirmation and hindsight biases) and questionable research practices (e.g.,p‐hacking, selective

censoring,undiscloseddatadredging, and flexible rules for terminatingdata collection).Althoughpre‐

registration has become standard practice in clinical medicine, it remains underutilized by emotion

researchers, perhaps reflecting nagging doubts about stifling scientific creativity or ‘extra paperwork.’

Neitherconcernholdsmuchwater.Pre‐registrationdoesnotprecludethepossibilityofserendipity—all

analysesremainfairgame(Poldrack,2016).Pre‐registrationsimplyforcesresearcherstobetransparent,

with ourselves and with others, about which results were genuinely predicted and which are new

discoveries (or a posteriori explanations) in need of replication. Once a study has been devised, pre‐

registrationiscomparativelypainlessusingweb‐basedtoolsmaintainedbytheOpenScienceFoundation

(https://osf.io)orothergroups(e.g.,https://clinicaltrials.gov).

Performing studies with inadequate statistical power represents another, perhaps more widely

recognized,waytofoolourselvesandadangertoreproduciblescience(Munafòetal.,2017;Poldracket

al.,2017).What is lesswellappreciatedisthat lowpowerdoesnot just increasethe likelihoodof false

negatives (‘null results‘), it also increases theprobabilityof falsediscoveriesandproducesoverly rosy

estimatesofeffectsize(Buttonetal.,2013a,2013b;Cohen,1992;Yarkoni,2009;Yarkoni&Westfall,in

press), a lesson learned the hard way by geneticists over the past decade (Bastiaansen et al., 2014;

Culverhouseetal.,inpress;Iacono,Vaidyanathan,Vrieze,&Malone,2014;Okbay&Rietveld,2015).Low

poweroftenreflectsalackofresources(e.g.,funds,time,accesstospecialpopulations),ratherthanalack

of knowledge; after all, software for computing power is freely available and power estimates are

required formostgrantapplications.Thischallenge isnotnecessarilyeasilyaddressed,givenresource

constraints, but inmany cases, canbe circumventedby teamscienceapproaches, consortia, andother

kindsofdatasharing.Theseapproachesareparticularlywell‐suitedtoareaswherethemeasurescanbe

Fox/Shackman,Epilogue10readily collected and quantified using standardized techniques (e.g., surveys of emotional traits, and

anatomicalMRIdata).

OpenReportingandSharing.Inthesamecommencementaddress,Feynmanunderscoredasecondkey

principle,theneedforfulldisclosurewhencommunicatingscientificresearch:

“…theideaistogivealloftheinformationtohelpothersjudgethevalueofyourcontribution;notjustthe

informationthatleadstojudgmentinoneparticulardirectionoranother”(Feynman,1974,p.11).

Providingacompleteandtransparentreportofthemethodsusedinaparticularstudyhasanumberof

benefits. Itenablesotherresearchersto fairlyevaluatethemeritsand limitationsof thework, tomore

readily reuse the methods in their own work, and to unambiguously incorporate the results into

narrativereviewsandmeta‐analyses(Munafòetal.,2017).Publicrepositoriesandothernewtoolsmake

iteasytogoastepfurtheranddirectlysharedata,code,andresults(e.g.,thresholdedmapsfrombrain

imaging studies;http://neurovault.org). Shareddataand results canbe combinedand reused innovel

ways.Opensourcecodecanbeexamined,corrected,andrefinedinwaysthatareimpossiblewithclosed

programs (Cox, Chen,Glen, Reynolds,&Taylor, 2017; Eglen et al., 2017; Eklund,Nichols,&Knutsson,

2016,2017).Publicsharingalsomakesiteasiertorecreateoldexperimentsandanalyses,evenwhenthe

personwhospearheadedtheprojecthasmovedon(Eglenetal.,2017).

Fox/Shackman,Epilogue11Although the replication crisis provides new urgency, the spirit motivating these four specific

recommendations—pre‐registration, power, reporting, and sharing—is not new. Skepticism,

transparency, and communalism (‘sharing’) are all longstanding scientific values (M. S. Anderson,

Martinson,&DeVries,2007;Merton,1942/1973)andconcernsaboutstatisticalpowerhavebeenvoiced

formore than a half‐century (Cohen, 1962).What has changed is thedevelopment of awide range of

digitaltoolsthatmakeadoptioneasierthanever.Embracingalloftheserecommendations,orevenone

ortwo,promisestoincreaseefficiency,enhancereproducibility,andaccelerateourunderstandingofthe

natureofemotion.

ClearNomenclature

Scientistshavelongrecognizedthatthewordsweusetodescribenaturehavethepowertoilluminateor

toobfuscate.FrancisBacon,oneoftheoriginalarchitectsofthescientificmethod,wrotethatthe“shoddy

andineptapplicationofwordslayssiegetotheintellectinwondrousways…wordsclearlyforcethemselves

on the intellect, throw everything in turmoil, and side‐track men into empty disputes, countless

controversies, and complete fictions" (Barber, 2017, p. 500). Four hundred years later, Poldrack and

Yarkoni made nearly the same point, arguing that “many of the theoretical disputes that arise in

psychology are…driven to a large extent by tacit differences in terminology that ramify as substantive

disagreements”(Poldrack&Yarkoni,2016).

Understandingthenatureandoriginsofemotionrequiresthatresearchersdescribeemotionsinaclear

andunambiguousway.Yet,aswithotherareasofpsychologyandneurobiology, this israrelythecase.

Since the publication of the first edition of this volume, a growing number of commentators have

Fox/Shackman,Epilogue12highlightedproblemswiththelanguageusedtodescribeemotionperception(Schaafsma,Pfaff,Spunt,&

Adolphs,2015);emotionalstates(LeDoux,2015;Shackman&Fox,2016b);stress(Kagan,2016a,2016b;

Koolhaasetal.,2011;Romeroetal.,2015);emotional traits (Block,1995;Morrison&Grammer,2016;

Nigg,2017;Poldrack&Yarkoni, 2016; Sharma,Markon,&Clark,2014); andemotional symptomsand

disorders,suchasanhedoniaanddepression(Zald&Treadway,2017).Thecommonrefrainacrossthese

commentariesisthat“seeminglyharmlessdifferencesinnomenclature”(Zald&Treadway,2017,p.476)

obscure important differences in neurobiology and phenomenology, impeding the development of

cumulativeknowledge.

Thispervasiveproblemreflectsseveralsemanticsins,includingtheuseofdifferenttermstorefertothe

same idea (jangle fallacy; Thorndike, 1904) and a single term to refer tomultiple ideas (jingle fallacy;

Kelly,1927).Takethecaseoffear.Nakedandunadornedwithinformationaboutantecedentsorcontext

(e.g., imminence of threat, possibility of escape), the word fear is insufficient for clear scientific

communication.LikeotherEnglishwordsforemotion,itcan,andoftenis,usedtorefertotheperception

of fearful or threatening stimuli, the expression of a range of defensive responses to threat, and the

experience of fearful feelings, three processes that reflect overlapping but qualitatively distinct neural

circuits(R.J.Davidson,1993;LeDoux,2012,2014,2015,inpress).Amongscientistsandlaypeople,fear

referstoabroadspectrum—or‘family’(http://atlasofemotions.org;Ekman,1994a;Ekman&Davidson,

1994)—of subjective states, frommortal danger to existential angst, and there is ample evidence that

these fearful states reflectpartiallydissociableneural systems (Blanchard,Griebel,&Blanchard,2001;

Calhoon&Tye,2015;Fanselow&Lester,1988;Fox&Shackman,inpress;Kalin&Shelton,1989;Mobbs

etal.,2007;Shackman&Fox,2016b).Preliminaryattemptstonamethesesystemshavefallenpreytothe

Fox/Shackman,Epilogue13sinofinconsistentusage.Inspiredbyevidencethatfear,likerewardandaggression1,canbefractionated

onetiologicalgroundsintoatleasttwokinds,agrowingnumberofresearchersdrawasharpdistinction

betweenfear(aphasicresponsetoimminentdanger)andanxiety(asustainedresponseintheabsenceof

imminentdanger;e.g.,Barlow,2000;Davisetal.,2010;LeDoux,2015;Tovote,Fadok,&Luthi,2015).In

fact,aversionofthisdichotomyisnowembodiedintheNational InstituteofMentalHealth’sResearch

DomainCriteria(RDoC)asAcuteThreatandPotentialThreat(Kozak&Cuthbert,2016)2.Confusionarises

fromthefactthat laypeople,scholarsinotherareas,theAmericanPsychiatricAssociation’sDiagnostic

andStatisticalManual (AmericanPsychiatricAssociation,2013),psychometricians(Kotovetal.,2017),

and even domain experts—at least in unguarded moments—use these terms interchangeably or

inconsistently (Kagan, in press;Watson, Stanton, & Clark, in press). Even the seemingly more precise

phrase‘diffuse,uncertain,orremotethreat’isusedtorefertoabewilderingarrayofparadigms,from15

minutesofexposuretoaunfamiliararenainrodentstoaseveralsecondsofuncertainanticipationofan

aversiveimageinhumans(Shackman,Tromp,etal.,2016).TheupshotisthatEnglishlanguagewordsfor

emotion—anger, fear, disgust, joy, sadness and so on—and even more recently coined phrases, like

‘uncertain threat,’ can, andoftendo, refer tomultiple phenomena (Wager,Krishnan,&Hitchcock, this

volume;Barrett,2017;Kagan,2010)andassuchrepresentapoorguidetotheunderlyingmechanisms.

Sowhatistobedone?Therewillalwaysbeaplaceforverbalshorthandandsosomeoftheseproblems

areinevitable,butwecaneasilydomuchbetter.Weurgeemotionresearchersto:

Bemindfulofthejingleandjanglefallacieswhenconsideringtheemotionliterature 1Aggressioncanbesplitonfunctionalandneurobiologicalgroundsintosystemsinvolvedindefensive,offensive(predatory),andconspecificaggression,withthelatterincludingmaternalaggressionandresourcecompetition(food,mates,andterritory/shelter)(Adams,2006;Berkowitz,1993;R.J.Nelson&Trainor,2007). 2Seealsohttps://www.nimh.nih.gov/research‐priorities/rdoc/constructs/potential‐threat‐anxiety.shtml;https://www.nimh.nih.gov/research‐priorities/rdoc/negative‐valence‐systems‐workshop‐proceedings.shtml.


Eschewproblematicredefinitionsofeverydaylanguage

Minimize or eliminate misleading single‐word descriptors, such as fear, that lump together

multipleprocessesandsubstrates.

Bewareofreification—theindexisnottheconstruct(Kagan,1988;Kendler,2016).Donotconfuse

‘fear’withpotentiationofthestartlereflexorfreezingintheelevatedplus‐maze.

Accurately specify thespecificparametersof theantecedent stimuli, the context inwhich those

stimuli are encountered, and the subsequent pattern of responses. Scientific constructs (e.g.,

gravity),gainstrengthwhentheyarecloselytiedtoempiricalmeasurements(Marx,1951).

Insomecases,aswithstimuliorresponsesthatvaryindegree(e.g.,physicalimminenceofthreat,

intensityofthermalstimulation,magnitudeofmonetaryreward),itwillbefruitfultodevelopand

usecomputationalmodels,whichenabletheuseofunambiguousmathematicalexpressionsthat

makeprecisepredictions.

RigorandRealisticInference

Drawing strong inferences about emotions, their underlyingneurobiology, and their consequences for

cognition,decision‐making,interpersonalprocesses,andotherpsychologicalprocesses,demandstheuse

of carefully designed experimental paradigms, psychometrically sound measures, intelligent analytic

choices, and sober interpretation of the results (Luck, 2005; Shackman et al., 2006; Tomarken, 1995).

Tasksorconditionsmustbewellequatedformotorrequirementsandperceptualcharacteristics.Insome

cases, psychometric matching will be fruitful. Affect is notoriously fleeting and induction procedures

typicallyfailtoelicitthetargetaffectinasubsetofsubjects(Shackmanetal.,2006).Thus,itisimperative

thatthepresenceofthetargetemotion(s)beverified.Emotionalstatesdifferintheirintensityaswellas

their persistence, which makes it crucial to understand the chronometry of affective responses (R. J.

Fox/Shackman,Epilogue15Davidson, 1998; Shackman, Tromp, et al., 2016; Tracy, Klonsky, & Proudfit, 2014). Emotionmeasures

oftenshowweakcoherenceand,thus,itisusefultoacquireseparatemeasuresofemotionalexperience,

peripheralphysiology,andbehavior(Bradley&Lang,2007;Ekman&Davidson,1994;Mauss,Levenson,

McCarter,Wilhelm,&Gross, 2005; Shackman et al., 2013). Investigators should be especially cautious

whencomparingresponses,whetherneuralorbehavioral,acrosstasksthatmarkedlydifferinduration

ornumberoftrials(i.e.,inthevarianceoftheread‐out),asinparadigmswherelongblocksarecompared

tobriefevents.

Parametric manipulations of the emotion‐eliciting stimuli (e.g., probability, duration, magnitude, or

intensity) can be especially powerful. Strong claims of specificity require comparison with an

appropriately arousing control condition. To draw strong inferences about disgust, for example, one

needs to contrast the effectswith those associatedwith an equally intense state of anger, fear, or joy.

Likewise,strongclaimsaboutpositiveaffectdemandcomparisonwithanequallypotentstateofnegative

affect.Moregenerally,inferencesaboutspecificityorconstructvalidityrequirecomparisonwitharange

of other tasks and conditions (Passingham, Stephan,&Kotter, 2002; Poldrack et al., 2017; Tomarken,

1995). Putative double dissociations need to be rigorously assessed by testing the appropriate

interaction(e.g.,RegionxCondition,ERPComponentxCondition,EmotionxCognitiveTask;Shackman,

Maxwell,McMenamin,Greischar,&Davidson,2011;Shackmanetal.,2006;Somerville,Whalen,&Kelley,

2010). Investigators shouldbe circumspectwhen interpretingunusually strongeffects (Lakens,2017).

Concludingthataparticularbrainregionis‘notinvolved’insomethingascomplexandmulti‐dimensional

as an emotion based on a significant difference in activity, a null test, or a single assay is completely

unwarranted. For neurophysiological techniques, such as functional MRI (fMRI) and

electroencephalography(EEG), trial‐by‐trialrelationsbetweenneuralsignalsandemotionalexperience

provide some of the strongest and most direct links between the brain and emotion (Atlas, Bolger,

Fox/Shackman,Epilogue16Lindquist, & Wager, 2010; Cavanagh & Shackman, 2015; Lim, Padmala, & Pessoa, 2009). Machine‐

learning techniques, though not without their limitations (Paulus, 2015; Woo et al., 2017; Yarkoni &

Westfall,inpress),providenewopportunitiesforidentifyingpatterns(e.g.,neuralactivation,symptoms,

behaviors)thatrobustlypredictemotionalstates,traits,anddisorders.Regardlessofapproach,itwillbe

increasingly important to employ techniques that examine the generalizability of our findings (e.g., by

cross‐validatingpredictionsacross rather thanwithin subjects). In summary, for optimal progress,we

mustbeclearwhatwearestudying,testourclaims,andacknowledgethelimitationsofourresearch.

Emotions vary in important ways across sexes and cultures (e.g., Chiao, this volume; Shansky, this

volume).Yet,scientistsoftenmakefundamentalclaimsaboutthenatureofemotiononthebasisofdata

drawnfromanarrowsliceofthisdiversity.Thevastmajorityofhumanstudiesrelyonindividualsdrawn

fromWestern,educated,industrialized,richanddemocratic(WEIRD)societies—whorepresentperhaps

asmuchas80percentoftheparticipantsinbiopsychosocialresearch,butonly12percentoftheworld’s

population(Henrich,Heine,&Norenzayan,2010)—andlaboratorystudiesofanimalsdisproportionately

rely onmale rats andmice (Institute ofMedicine, 2001).Whether the fruits of thiswork translate to

‘everyoneelse’remainsunclear.Asimilarconcernappliestotheissueofmeasurementcontext(Ekman&

Davidson,1994;LeDoux,2014).Thecontext inwhichanemotioniselicitedcantransformtheemotion

that is experienced (e.g., anger vs. fear), the way in which it is expressed (e.g., freezing vs. flight vs.

defensiveattack),andthebraincircuitsthatsubserveit(Blanchard&Pearson,thisvolume;Kagan,this

volume; Barrett, 2017; Kagan, in press;Khalsa et al., 2016; LeDoux, 2014;Wager & Atlas, 2015). Yet,

laboratory studies of emotion rely on a narrow range ofmeasurement contexts (e.g., lying alone in a

scanner).Studentsofemotionshouldberealisticabouttheirconclusionsandnotassumethatinferences

derivedfromonecontextorgroupwillnecessarilyproveuniversal.


CoordinatedCross‐SpeciesResearch

MuchoftheneurobiologicaldatareviewedintheNatureofEmotioncomesfromhumanEEGandimaging

studies.Themostcriticallimitationofimagingstudiesisthattheyarecorrelationalandcannotaddress

causation.Fullyaddressingthischallengemandatesmechanisticstudiesinhumansandanimals,aswell

ascoordinatedcross‐speciesresearchefforts.Animalmodelsenableadegreeofresolution,precision,and

control that are nearly impossible to achieve in studies of humans. In contrast, human studies are

essential for understanding the precise neural mechanisms supporting the subjective experience of

emotions (D. J. Anderson & Adolphs, 2014; LeDoux, 2015) and for identifying the features of animal

modelsthatareconservedand,hence,mostrelevanttounderstandinghumanemotionaldisordersand,

ultimately,todevelopingimprovedinterventionsforhumansuffering('forwardtranslation;'Birnetal.,

2014; Hyman, 2016). Human studies also afford important opportunities for developing objective

biomarkersofdiseaseordiseaserisk(Wooetal.,2017)andforgeneratingnovelhypothesesthatcanbe

mechanisticallyassessedinanimalmodels('reversetranslation’).

In animalmodels, focal perturbation techniques can be combinedwith the samewhole‐brain imaging

strategies routinely applied in humans, facilitating the development of integrated, bidirectional

translationalmodels(Borsook,Becerra,&Hargreaves,2006;Caseyetal.,2013;Desaietal.,2011;Foxet

al., 2010;Grayson et al., 2016;Kalin et al., 2016).This combined approach is particularly valuable for

determining whether changes in emotional behavior are mediated by alterations in the function of

downstream regions, as occurs followingOFC lesions inmonkeys (Fox et al., 2010)orOFCdamage in

humans (Motzkin, Philippi, Oler, et al., 2015). Combining cognitive‐behavioral, neurofeedback,

neurostimulation,orpharmacologicalinterventionswithfMRIorEEGinhumanscanprovideadditional

Fox/Shackman,Epilogue18opportunities for understanding the neural mechanisms underlying the experience and expression of

emotion (Duff et al., 2015; Lapate et al., in press; Paulus, Feinstein, Castillo, Simmons, & Stein, 2005;

Schnyeretal., 2015;Sitaramet al., 2017). Similarly, imagingapproaches canandshouldbeapplied to

rare patients with circumscribed brain damage (Adolphs, 2016; Motzkin, Philippi, Oler, et al., 2015;

Motzkin,Philippi,Wolf,Baskaya,&Koenigs,2014,2015;Spuntetal.,2015).

Oncewe establish candidate proximal causes for a particular emotion,we can begin to address some

other crucial questions. For example, how specific is this circuitry (at the neuronal, voxel, or regional

levels;Passinghametal.,2002;Pessoa,2017;Wooetal.,2017;Zaki,Wager,Singer,Keysers,&Gazzola,

2016)?How is it related tomorepersistent affectivephenomena, such asmoods and emotional traits

(Shackman,Tromp,etal.,2016)?Addressingspecificityisparticularlyimportantforunderstandinghow

emotionisintegratedintocognition,decision‐making,andsocialprocessesandwouldprovidevaluable

clues about why disparate features of emotion, such as vigilance and worrisome thoughts (Grupe &

Nitschke,2013)oranxietyandconflictmonitoring(Cavanagh&Shackman,2015),oftenco‐vary.Itwould

also help to address on‐going debates about the degree towhich emotions reflect specialized centers,

domain‐generalmodules,orsomecombinationofthesebuildingblocks(Adolphs,2017;Barrett,2017).

EmotionsintheRealWorld

Physiological studiesofemotionhavereliedheavilyona limitednumberofwell‐controlled,buthighly

artificial manipulations—static faces, sounds, images, small monetary rewards, and so on—presented

under unnatural conditions. Subjectsmay, for example, be instructed to passively view a randomized

streamofpositiveandnegativephotographswhilelyingmotionlessinthecramped,dimlylitconfinesof

Fox/Shackman,Epilogue19anMRIscanner.Byandlarge,thesemanipulationsarefarlessarousingandmuchlessengagingthanthe

kinds of antecedents regularly encountered in daily life or those routinely used in animal models

(Levenson,thisvolume;LeDoux,2015;Levenson,2011;Shackmanetal.,2006).Althoughthisapproach

has afforded a number of important insights, it is unclear howmuch of this knowledge is relevant to

emotionintherealworld—inthebedroomandtheclassroom,theboardroomandthebar.

Given the limitations of ambulatory measures of brain activity—there is no ‘fMRI helmet’ as yet—

addressing this question requires integrating assays of brain function and behavior acquired in the

scannerwithmeasuresofemotionandmotivatedbehaviorassessedundermorenaturalisticconditions

in the laboratory (e.g., during semi‐structured interactions;Creed&Funder, 1998; Laidlaw, Foulsham,

Kuhn,&Kingstone,2011;Perez‐Edgaretal.,2010;Pfeiffer,Vogeley,&Schilbach,2013)orinthefield,a

pointalsomadebyEkmanandDavidsoninthefirsteditionofTheNatureofEmotion(Ekman&Davidson,

1994).Recentworkcombining fMRIwithexperience‐sampling techniquesunderscores thepotentialof

this approach for identifying the neural systems associated with naturalistic variation in mood and

motivated behavior—a central goal of psychology, psychiatry, and the behavioral neurosciences

(Berkman & Falk, 2013; Forbes et al., 2009; Heller et al., 2015; Lopez, Hofmann, Wagner, Kelley, &

Heatherton,2014;Wilson,Smyth,&MacLean,2014).Prospective longitudinaldesignswouldprovidea

valuable opportunity to discover the relevance of specific emotional circuits in the brain to the

development of maladaptive mood and pathology‐promoting behaviors, such as avoidance and social

isolation(Admonetal.,2009;McLaughlinetal.,2014;Swartz,Knodt,Radtke,&Hariri,2015).

Thedevelopmentof robustmobileeye trackers, theemergenceof commercial software forautomated

analyses of facial expressions (Olderbak, Hildebrandt, Pinkpank, Sommer, &Wilhelm, 2014), and the

Fox/Shackman,Epilogue20widespread dissemination of smart‐phone and other kinds of ‘wearable’ technology for adults and

childrenaffordadditionalopportunitiesforobjectively,efficiently,andunobtrusivelyquantifyingcontext,

emotion,andmotivatedbehaviorinvivo(Gilmore,2016;Gosling&Mason,2015;Onnela&Rauch,2016;

Sano et al., 2015; Wrzus & Mehl, 2015). Combining these measures with laboratory assays of brain

functionandperipheralphysiology(e.g.,emotion‐modulatedstartle)wouldprovidenovelcluesaboutthe

neuralsystemssupportingmoodandmotivatedbehavior indaily life,closetoclinicallyandpractically

importantend‐points.Thisapproachpromisesadepthofunderstandingthatcannotbeachievedusing

eitheranimalmodelsorisolatedmeasuresofbrainfunction.Evenintheabsenceofbiologicalmeasures,

thesenewtoolspromiseimportantcluesaboutthedynamicsofemotionalstatesindailylife(e.g.,spill‐

overofmoodacrosssequential contextsandassessments)and thesocial factorsandcopingbehaviors

that help govern the momentary expression of emotional traits (Shackman, Tromp, et al., 2016;

Shackmanetal.,inpress;Tambini,Rimmele,Phelps,&Davachi,2017).

SPECIFICCHALLENGESFORFUTURERESEARCHINTHEAFFECTVESCIENCES

The 92 essays thatmake up the present volume tell uswhatwe as a field know about the nature of

emotion.Buildingonthisfoundation,inthisthirdandfinalsectionoftheEpilogue,wehighlightsomeof

themostimportantsubstantiveareasforfutureresearchintheaffectivesciences.

TheIntegrationofEmotionandCognition

Emotion and cognition can seem quite different at first glance. Emotion is infused with feelings of

pleasureorpainandmanifests inreadilydiscernedchanges inthebody,whilecognitionoftenappears

devoid of these features. From classical times to the present, these apparent differences in

Fox/Shackman,Epilogue21phenomenological experience and peripheral physiology have ledmany scholars to treat emotion and

cognition as categorically distinct, even oppositional, mental faculties (Barrett, 2017; de Sousa, 2014;

Schmitter,2014).Asimilardichotomypervadespsychiatricnosology.Butwiththeadventofnewtools

fornoninvasivelyassayingthebrain,theideathatemotionandcognitionaredifferentinkindbeganto

dissolve(Okon‐Singer,Hendler,Pessoa,&Shackman,2015).AtthetimeTheNatureofEmotionwasfirst

published,in1994,onlyafewcommentatorsemphasizedtheneuralintegrationofemotionandcognition

(R. J. Davidson, 1994; Lazarus, 1991). A quarter century later, there is widespread agreement that

emotionandcognitionaredeeplyinterwoveninthefabricofboththemindandthebrain(Questions1,5,

and8).Thisshouldnotbesurprising—afterall,thehumanbraindidnotevolvetooptimizeperformance

onlaboratorymeasuresof‘cold’cognitionortopassivelyrespondtoexperimentalmanipulationsof‘hot’

emotions.Ourbrain,likethatofotheranimals,istheproductofevolutionarypressuresthatdemanded

neural systems capable of using information about pleasure and pain, derived from stimuli saturated

withhedonicandmotivationalsignificance,toregulateattention,learning,andbehaviorintheserviceof

maximizingfitness.

Despite this progress, a number of important questions remain unresolved. For example, what is the

functional significance of regions—like the anterior insula, mid‐cingulate cortex, and dorsolateral

prefrontal cortex—that are recruited by both cognitive and affective challenges (e.g., de la Vega et al.,

2016;Shackman,Salomons,etal.,2011).Doesthisreflectasingleinvariantfunctionormultiplefunctions

(i.e.,functional‘superimposition’ormoredynamickindsofmultiplexing)?Doesthefunctiondependon

the state of the larger networks in which these regions are embedded? Another general question

concerns the relationship between emotions, on the one hand, and the kinds of functional circuits

identifiedbycognitiveneuroscience,ontheother.Howisthreat‐relatedvigilance,forexample,relatedto

thecircuitry thatunderliessustainedattention(Davis&Whalen,2001;Shackman,Kaplan,etal.,2016;

Fox/Shackman,Epilogue22Shackman,Maxwell,etal.,2011)?Howdoesruminationrelatetoshort‐andlong‐termmemorysystems?

Addressing these questions is practically, as well as theoretically, important and would inform our

understandingofpsychiatricsigns(e.g.,threatover‐generalization,aberrantreinforcementlearning)and

disorders(e.g.,schizophrenia)thatlieattheintersectionofemotionandcognition.

ControllingOurEmotions

There have been tremendous advances in our scientific understanding of how thinking can exert

bidirectionalcontroloveremotion(Questions5,7,and8).Cognitivereappraisalisrecognizedasameans

for deliberate emotion regulation and has had success as a core component of many treatments for

emotionaldisorders(Gross,2014).Thereisclearevidencethatrumination,worry,andhopelessnesscan

maladaptivelypromoteandmaintainnegativeaffectandcancontributetothedevelopmentofmoodand

anxietydisorders(Barlow,Sauer‐Zavala,Carl,Bullis,&Ellard,2013;Hyde,Mezulis,&Abramson,2008;

Nolen‐Hoeksema,Wisco,&Lyubomirsky,2008;Watkins,2008).Despitethisprogress,itisclearthatwe

haveonlyscratchedthesurfaceofemotionregulation.Anumberofcontributorsdiscussedhowthinking

cangenerateandtransformemotions.AkeenexamplecomesfromCarolineBlanchard’sstoryofhowshe

“sleptfornearlytwoyearswithascarftiedaroundherneckafterreadingBramStoker’sDraculaatan

unwisely precocious age” (Blanchard& Pearson, this volume). This childhood anecdote highlights the

power of cognition—oftenpassed fromperson‐to‐person through story, conversation, and thewritten

word—totriggerstrongemotionsandmotivateenduringbehavioralchanges.Weinvitereaderstoreflect

onwhatthisimpliesaboutthelimits(orlackoflimits)—onourcapacitytouseourthoughtstocontrol

ouremotions.

Fox/Shackman,Epilogue23Thoughtscannotonlygenerateanemotionalresponse,buttheycanalsomodulatethetypeofemotion

thatisprovoked.Forinstance,thoughtscanbridgebetweencontextandcontext‐appropriateemotions.

For example, asMaoz & Bar‐Haim note, our feelings about a colleague running late to ameeting are

inherentlylinkedtoourthoughtsabouthernormalbehavior,andcanrangefromangerandfrustration

(ifsheishabituallylate)toconcernandapprehension(ifsheishabituallypunctual)(Maoz&Bar‐Haim,

this volume).More generally, thoughts can transform thenatureof an emotional stimulus.Adelicious

juice can quickly become disgusting following exposure to a perceived contaminant, such as a bug or

bedpan (even after it has been sterilized!) (Rozin, Haidt, & McCauley, 2008). Moreover, this disgust‐

linked contamination changes across development, enabling older children to become disgusted by

increasinglyabstractideas(e.g.,aswastikaorklansman’swhitehood)astheircognitiveabilitiesmature

(Rozin et al., 2008). These data underscore the intimate links between cognition and emotion, and

reaffirmtheabilityofthoughtsandideastocontrolourfeelings.

In short, our thoughts are linked to our emotions along the entire cascade of emotionprocessing and

across a range of time‐scales. A significant challenge for affective scientists is to develop a deeper

understandingofpreciselyhowthesecognitiveappraisalsinemotionalprocessingoperate.Forexample,

relatively little is known about the more elementary cognitive processes that underlie appraisal and

appraisal tendencies (but cf. Scherer, 2009). What role do trait‐like appraisal tendencies play in

determiningaffective‐styleandtowhatextentare theseprocessessusceptible tovoluntaryorhabitual

training?Onehintthattrait‐likeappraisaltendenciescanchangecomesfromtheworkofCarstensenand

colleagues, who suggest that a changing appraisal of the subjective sense of time left on this planet

mediates the increases inwell‐being seenduringold‐age (Carstensen, this volume).Reconceptualizing

andelucidating theappraisalprocess to include these long‐lastingappraisalscanprovidea framework

Fox/Shackman,Epilogue24fornew,andpotentiallyrevolutionary,methodstomanageandregulateemotions,andtreatemotional

disorders.

InfluencingOthers’Emotions

Emotionisprofoundlysocial(Questions9‐10).Emotionalexperiencesareroutinelysharedanddissected

with friendsand family (Rime,2009)andsocial engagement tends topromotepositiveaffect (Clark&

Watson, 1988a, 1988b;Watson, 1988; Watson, Clark, McIntyre, & Hamaker, 1992). Most attempts at

emotionregulationoccurinsocialcontexts(Gross,Richards,&John,2006)andthereisampleevidence

that close companions play a vital role in copingwith stress and regulating negative affect (Bolger &

Eckenrode, 1991;Myers, 1999). Individualsdiffer in their ability to capitalize on these kinds of socio‐

emotionalsupport(Shackmanetal., inpress)andthosepronetolonelinessandlowlevelsofemotional

intimacy aremore likely to experience adverse outcomes, such as divorce and depression (Cacioppo,

Grippo, London, Goossens, & Cacioppo, 2015; Editors, 2010; Kendler & Halberstadt, 2013; Shackman,

Tromp, et al., 2016). In short, it is clear that other individuals can, and frequently do, influence our

emotionsinavarietyofimportantways(Coan&Sbarra,2015;Zaki&Williams,2013).

Of course, interpersonal processes are a two‐way street, creating numerous opportunities for the

bidirectional control of emotion. Parents and teachers, spouses and therapists, entertainers and

politiciansall leverage thecapacity to strategically regulate theemotionsofothers tovaryingdegrees,

butwehaveonlyjustbeguntodevelopascientificunderstandingoftheunderlyingmechanisms(Reeck,

Ames, & Ochsner, 2016). Intentionally managing others’ emotions may depend on the same kinds of

techniques commonly applied to the self‐regulation of emotion, including situation selection and

Fox/Shackman,Epilogue25modification, distraction, cognitive reappraisal, and response modulation (Reeck et al., 2016). Recent

workalsohighlights thepossibilityofdeliberatelycultivatingstates,suchascompassion, thatpromote

prosocial responses to others suffering and distress (Engen & Singer, this volume; Stellar & Keltner,

2014;Weisz&Zaki, inpress;Wengetal., 2013).Allof these regulatory strategies criticallydependon

accuratelyinferringothers’emotions,oftenonthebasisoflimitedorambiguousinformation(Question

10).Becausetheverynatureofperceptioncanbesusceptibletotheinfluencesofstereotypesandbias,it

will be critical to develop techniques to overcome biases in active perception. Developing a deeper

understanding of the underlying perceptual, computational, and neurobiological mechanisms that

support interpersonal regulation of emotion is important and would guide the development of novel

interventions focused on dyads (e.g., parents and their offspring) and other more complex social

networks (Baucom, Belus, Adelman, Fischer, & Paprocki, 2014; Chronis‐Tuscano et al., 2015; Kok &

Singer,2017;Marroquin,2011).

ExpandingthePhysicalBasesofEmotion

Scholarshavelongrealizedthatitisproblematictoconsideremotionwithouttakingsignalsfromthe

bodyintoaccount.Classicalperspectivesonphysicalembodimentfocusontransientchangesinthe

expressivemusclesoftheface,theheart,andtheperipheralnervoussystemthatpreparethebodyto

adaptivelyrespondtoacuteemotionalchallenges(Damasio&Damasio,thisvolume;Wood,Martin&

Niedenthal,thisvolume;LeDoux,2015).However,ithasbecomeclearthatweneedtoexpandthese

classicalperspectivesonembodiment.Whileourcentralnervoussystemevolvedtoemote(Fox,this

volume),otherbodilysystemsandorganismsseemtohaveevolvedthecapacitytoinfluenceour

emotions,somethingnotaddressedbyexistingtheoriesofemotion.Futuretheorieswillneedtoaccount

fortheinfluenceoftheimmunesystemaswellasthemanytrillionsofmicroorganismsthatliveonand

Fox/Shackman,Epilogue26withinourbodies.Sicknessbehavior—whichischaracterizedbyoutwardsignsthataresimilarto

depression,includinglethargy,apathy,andadesiretobealone—providesanexcellentandrelatively

well‐understoodexampleoftheimmunesystem’sroleingoverningmoodandemotionalbehavior

(Rosenkranz,thisvolume).Likewise,thecuriouscaseoftheparasitetoxoplasmagondiiprovides

compellingevidencethatmicroorganismscandramaticallyinfluencemotivatedbehavior(Rosenkranz,

thisvolume;House,Vyas,&Sapolsky,2011;Vyas,Kim,Giacomini,Boothroyd,&Sapolsky,2007).T.gondii

canonlysexuallyreproduceinthecatgut.Theproblemisthattheyareregularlyexcretedandtherefore

requireanintermediatehost,suchasabirdorrodent,tomaketheirwayback.Afterinfectingtheir

intermediatehost,T.gondiialterthehost'sneuralresponsetocatodor,changingtheirinnateaversionto

attractionandincreasingthelikelihoodthatacatwilleattheintermediatehost.Thesekindsof

observationstellusthattheuniverseofinteractionsbetweenemotionandthebodyisvastlylarger,

considerablymorecomplex,andcanplayoutovermuchlongerspansoftimethanJamesandLange

probablyhadinmind.Inparticular,theyhighlighttheneedtoexpandembodiedmodelsofemotionto

encompassabroaderspectrumofperipheralbiology,includingtheimmunesystemandthebody’s

microbiome.

EmotionsandDecision‐Making

Another major development since the initial publication of this volume has been the realization that

affective processes are central to value‐based decision‐making. The observation that optimal and

adaptivedecisionsrelyonaffectivevaluationratherthan‘coldcognition’wasanimportantadvancefor

bothaffectiveandeconomicscience.Duringthissamespan,asubstantialbodyofevidencehasamassed

to indicate that the neural systems underlying emotion largely overlap with those supporting value‐

baseddecision‐making; that emotion‐altering lesionsordrugs frequently changedecision‐making; and

thattask‐irrelevantemotioncanbiasdecisions(e.g.,Engelmann&Hare,thisvolume;Knutson&Stallen,

Fox/Shackman,Epilogue27this volume; Murray, this volume; Tymula & Glimcher, this volume. These data dovetail with earlier

observations that emotions help organisms choose adaptive behaviors that facilitate survival and

reproduction. Determining exactly how emotions influence decisions can feed‐back and inform our

understandingofemotionandhaspotentiallyimportantimplicationsforpublichealthandpublicpolicy,

withapplicationstoobesity,addiction,anddepression.

Looking to the future, it will be important to develop increasingly accurate models of choice that

incorporate the biasing influence of emotional states, traits, and disorders. Choices often hinge on

predictions about the value of potential outcomes. A number of contributors suggested that these

economicvaluationsignalscanbeconceptualizedasaformofaffect,andthatsimulatedemotionforms

the basis of value based decision‐making (e.g., Chang & Jolly, this volume; Engelmann & Hare, this

volume;Hartley&Sokol‐Hessner,thisvolume;Reber&Tranel,thisvolume).Achiefstrengthofdecision‐

making research has been the development of formal and precisemathematicalmodels that underlie

decision‐making. These models have allowed researchers to tease apart the hidden processes that

contribute to decision‐making, and search for their neural and psychological correlates. For example,

within the present volume specific decision‐weights have been associated with particular aspects of

emotion, including surprise (Friston, Joffily, Barrett, & Seth, this volume), guilt (Chang & Jolly, this

volume),andarousal (Hartley&Sokol‐Hessner, thisvolume).Amajorchallenge for the fieldwillbe to

understand the influence of emotions on the economic axioms of choice (Tymula & Glimcher, this

volume).Thiswillallowresearcherstopreciselyarticulatehowcurrenteconomicmodelsarewrongand

provide a clear guide forwhat adaptations to thesemodels are necessary to best account for human

behavior(e.g.,decision‐makingunderrisk,fairness)(Fehr&Schmidt,1999;Kahneman&Tversky,1979).

Fox/Shackman,Epilogue28The development of increasingly accurate models of decision‐making will provide insight into why

peoplemakemaladaptiveand/orselfishdecisions. Insight intohowweassignvaluetofoodanddrugs,

for example, haspromise forhelping to clarify theetiologyand treatmentof addiction, amajorpublic

health issue. Likewise, developing amore comprehensive understanding of prosocial valuation,would

guide potentially revolutionary developments of public policy focused on optimally incentivizing the

globalgoodandcollectivewell‐being(seethesectiononPlasticity,below).

TheDevelopmentofEmotionandtheImpactofDevelopmentalInsults

There iswidespreadagreementthatmost, ifnotall,aspectsofemotionchangeandmaturethroughout

development, from gestation through late life (Question 14). Yet, the precise nature ofmany of these

changesremainspoorlyunderstood.Itwillbenecessaryforaffectivescientiststodisentangleoftenco‐

occurring processes (e.g., changes in ‘emotional reactivity’ vs. ‘emotion‐regulatory’ systems; Crone &

Pfeifer,thisvolume),inordertounderstandthemechanismsofdevelopmentallyrelevantbiologicaland

psychologicalinsults,andintegrateemotionaldevelopmentwithmodernstatisticallearningtheories.

Parsing thecausalmechanismsunderlyingdevelopmental changes isdifficultbecausesocial, cognitive,

andbiologicaldevelopmentoftenoccur intandem.Thus,amajorchallengeforaffectivedevelopmental

research is todevelop toolsand techniques todissect thedistinct contributionsof changes inphysical

maturation(e.g.,braindevelopment,sexhormones),cognition(e.g.,selectiveattention,cognitivecontrol,

workingmemory), environmental stressors (e.g., new school), and new social roles (e.g., dating). For

example,doesteenageemotionallabilityresultfromprefrontal‐limbicimbalanceorincreasedexposure

tonewandunknownsituations(e.g.,Crone&Pfeifer,thisvolume)?Presumablyeachhasitsownimpact,

Fox/Shackman,Epilogue29butwewillneverknowwithoutintensivelongitudinalassessmentsofneurobiologyandcognitioninthe

laboratory,coupledwithecologicalassessmentsofreal‐worldemotionandsocio‐contextualinformation,

alongsidemechanisticstudiesofdevelopmentinnon‐humananimals.

There is ample evidence that biological and psychological insults (e.g., fetal exposure to maternal

sickness,physicalmaltreatment,deathofaspouse)canhaveenduringconsequencesforemotionalhealth

and well‐being as we develop. Unfortunately, because we know preciously little about the specific

mechanismsunderlyingtheinteractionbetweenthesedevelopmentalinsultsandthebrain,wegenerally

cannotpredicthowtheywillaffectanindividual,norcanweprescribeoptimaldevelopment‐orinsult‐

specific interventions. Therefore, an important goal of developmental affective research will be to

determine which components of emotion development are most susceptible to different kinds of

biologicalandpsychologicalinsults,anddeterminetheextenttowhichtheyarebetterconceptualizedas

temporarysetbacksoraslowingofdevelopment.

Finally, it will be fruitful to integrate theories of emotion development with generalized statistical

learning theory, which describes the process of using statistical regularities to learn about theworld

(Saffran,2003).Forexample,whenachildcriesashermother leaves, is itbecause theevent ishighly

aversive or because it is negative and surprising? Friston and colleagues’ theory of emotion, which

suggeststhatemotionsrepresentakindofpredictionerror,impliesthatthedevelopmentofemotionis

intricately intertwinedwith a child’s ability to accurately predict theworld (Friston, Joffily, Barrett,&

Seth,thisvolume).Thus,inthecaseofthechild,thesurprisemaybemorerelevantthantheaversiveness.

As childrendevelopbetterpredictions aboutwhen food is coming andwhenparentswill return, they

Fox/Shackman,Epilogue30mayceasetoexpressextremeemotionstothesecommonevents.Thisconceptualapproachprovidesa

uniquesetofhypothesesthatmayprovideinsightintothedevelopmentofemotionearlyinlife.

FeelingsandConsciousness

Moving forward, there is a great need to distinguish feelings—that is, the subjective experience of

emotion—from other components of emotion, such as alterations in peripheral physiology and action

tendencies. Feelings are a fundamental component of the everyday experience of emotion and have

intrinsic worth, as they form the basis of perceived well‐being and largely define various forms of

psychopathology.Subjectiveexperienceof feelingsrequiresaconsciousawarenessofongoingaffective

processing,and,importantly,consciousawarenessofemotion‐elicitingeventshasbeendemonstratedto

influenceneuralandbehavioralaspectsofemotionprocessing(Question12;LeDoux&Brown,2017).

Developing a deeper understanding of the role of conscious awareness in emotion is important and

promises to refine our thinking about the relations between emotions, feelings, and psychopathology

(LeDoux,2015).Inparticular,itwillbecriticaltoidentifytherelevanttypesofconsciousawarenessand

eachof their effectsonemotional responding. For example,while anumberof contributors suggested

that the conscious awareness of emotion‐eliciting events modulates neural responses and behavioral

consequences of emotional processing (Question 12), it remains unclear which aspects of conscious

awareness are essential: awareness of the emotion elicitor, awareness of the subsequent emotional

response (interoception), and/or of the link between the two (contingency or source‐of‐emotion

awareness).

Fox/Shackman,Epilogue31Moreover,althoughitiswidelyassumedthatconsciousawarenessoffeelingstatesiscriticalforemotion

regulation,andthatincreasingawarenessofemotionaltriggersisacriticalfactorfordistincttherapeutic

approaches(e.g.,psychotherapyandmindfulness),thenecessityofconsciousawarenessperse inthese

processes has rarely been rigorously tested. For example, is decision‐making more strategic when

accompanied by conscious awareness of emotional events that influence the decision? Further, does

awareness of peripheral‐physiological aspects of an emotional response promote emotion regulation

(e.g.,byfacilitatingrecoveryorareturntobaselineconditions)?Answeringtheseandrelatedquestions

willbeessentialforthedevelopmentofwell‐informedtheoriesofconsciousnessinemotionthathavethe

potentialtooptimizecognitive‐behavioralinterventions.

PlasticityandIntervention

Classicaltheoriesofaffectivestyle,temperament,andpersonalitywouldseemtosuggestthatthehuman

brain is static, certainly once adulthood is reached. But it has become increasingly clear that, like a

mature but growing tree, our brains are in constantmotion. Throughout our lives, new synapses are

beingcreated,newneuronsarebeingborn,existingconnectionsarebeingstrengthened,and,ultimately,

newthoughtsarebeinggenerated(Goldsmith,thisvolume;McEwen,thisvolume).Inparallel,evidence

thatemotionaltraitscan,anddo,changewithtimeandtrainingisbeginningtoaccumulate(e.g.,Roberts

etal.,2017).Likethemotorandvisualsystems,theemotionalbraincanchangewithexperience.Inthe

extreme,wecandevelopPTSDorlearntoenjoyrollercoasters.Morebroadly,measuresofdispositional

traitsonlyshowmoderatestabilityoverlongperiodsoftime,andalthoughaneuroticchildissomewhat

morelikelytobecomeaneuroticadult,theyarenotdestinedforthisfate(Borghuisetal.,inpress;Fraley

&Roberts,2005;Hakulinenetal.,2015;Milojev&Sibley,2017;Nye,Allemand,Gosling,Potter,&Roberts,

2016;Roberts&DelVecchio, 2000;Roberts&Mroczek,2008;Roberts,Walton,&Viechtbauer, 2006) .

Fox/Shackman,Epilogue32Themechanismsunderlyingthisplasticityremainunderexplored,makingitakeychallengeforthefield.

Although environmental influences, both good and bad, can modulate emotional traits (Shackman,

Tromp,etal., 2016), the limitsof these influences remainmostlyunknown.Moving forward, itwillbe

helpful for researchers to examine individuals exposed to more extreme cultural and environmental

changes(e.g.,adoption,emigration,enlistment).

Perhapsthemosttantalizingprospect isourcapacitytochangeinresponsetoexplicit interventionsor

training. Humans have learned to train our awareness, treat our anxieties, and practice being

compassionate (e.g., R.J. Davidson & Harrington; Hofmann & Smits, 2008; Lutz, Slagter, Dunne, &

Davidson, 2008). Scientists have observed that each of these interventions is associated with

correspondingchangesinneuralfunction(e.g.,Furmarketal.,2002;Tang,Holzel,&Posner,2015;Weng

etal.,2013).Thesedataremindus thatenduringchanges in themindnecessarilyreflectalterations in

protein synthesis and expression in the brain. These neuroplasticity related processes are, in turn,

relatedtoindividualdifferencesinemotionality,andcanbemodulatedbystressandexercise(e.g.,R.J.

Davidson&McEwen, 2012; Fox&Kalin, 2014; vanPraag, Christie, Sejnowski,&Gage, 1999). In adult

mice,forexample,neurogenesisisassociatedwithdecreasesinanxiety‐likebehavior, is increasedwith

exercise,andisrequiredforthebehavioraleffectsofantidepressants(Pereiraetal.,2007;Sahay&Hen,

2007;Santarellietal.,2003).Developingadeeperunderstandingoftheneuralmechanismsthatsupport

different forms of emotional plasticity is important and would inform the development of new,

biologically‐motivated pharmacological, cognitive‐behavioral, contemplative, and pharmacological

interventions(R.J.Davidson&Kaszniak,2015).

Fox/Shackman,Epilogue33Finally, although we often think of interventions as treatments aimed at healing the sick, several

contributors highlighted the possibility of emotional enhancements, the possibility of moving beyond

baselinelevelsofemotionalwell‐being(e.g.,Fredrickson,thisvolume;Ryff,thisvolume).Aswestrivefor

amorepeacefulandblissfulworld,amajorchallengeforaffectivescientistswillbetodeveloptraining

programsaimedatcultivatingcompassionandcontentment.

CONCLUSIONS

Emotion isa core featureof thehumancondition,with importantconsequences forhealth, forwealth,

andforwellbeing.Recentyearshavewitnessedgrowingenthusiasmforunderstandingboththenature

andthebiologicalbasesofemotion.Theresearchcontainedinthisvolumeprovidesadetailedsurveyof

the current state of the affective sciences andhighlights the important advances that havebeenmade

sincethepublicationofthefirstedition,nearlyaquartercenturyago.Someofthefundamentalquestions

originally posed by Ekman and Davidson have now been largely answered (e.g., “Can emotions be

regulated?”),while othershaveprovenmoreelusive (“What isanemotion?”). In some cases, there are

nowsufficientdatatoenablepreliminaryanswerstoentirelynewkindsofquestions(“Howareemotions

organizedinthebrain?”).Still,itisclearthatmostofthework,bothempiricalandconceptual,neededto

understandtheemotionsandrelatedaffectivephenomenaremainsundone.AmajorgoalofTheNatureof

Emotionistomotivatethecurrentandnextgenerationofaffectivescientiststodotheresearchandthe

thinkingthatwillberequiredtoaddresstheseoutstandingquestions,todevelopnewquestions,andto

generatemorecompleteandusefultheoreticalmodels.

Fox/Shackman,Epilogue34In this Epilogue, we have outlined some of the most important strategies and directions for future

researchintheaffectivesciences.Atthebroadestlevel,itwillbeimportanttodevelopamorecomplete

understanding of the mechanisms linking emotional antecedents to their consequents. When

appropriately grounded in behavior, neurobiological approaches promise to be especially valuable for

addressing thisandotherkeyquestions.Thewiderembraceofbestpractices—openandreproducible

science, clear nomenclature, rigorousmethods and realistic inferences—would increase the efficiency,

reproducibility, and inferential utility of emotion research. An increased focus on coordinated cross‐

species models would accelerate our understanding of mechanism and has the potential to provide

uniqueinsightsintothenatureofemotion.Integratinglaboratoryassaysofthebrainandbehaviorwith

measurescollectedinthefieldusingexperience‐samplingtechniques,ambulatoryphysiology,andother

kinds of smartphone‐enabled and ‘wearable’ technologies would provide important clues about the

neuralsystemssupportingemotionandmotivatedbehaviorindailylife—adepthofunderstandingthat

cannotbeachievedusinganimalmodelsorisolatedmeasuresofbrainfunction.Inthefinalsectionofthe

Epilogue,wehighlightedwhatweviewaseightofthemostexcitingandpotentiallyimpactfulavenuesfor

the next generation of emotion research. In particular, we believe that there is a deep need for

programmaticresearchfocusedonunderstandingthe:

Interplayandintegrationofemotionandcognition

Self‐regulationofourownemotions

Socialregulationofothers’emotions

Roleoftheimmunesystemandmicrobiomeinemotionregulationanddysregulation

Developmentofemotionandthenatureofdevelopmentalinsults

Natureofconsciousnessanditscontributiontosubjectivefeelings

Originsofemotionalplasticityandtheprocessesunderlyingeffectiveemotioninterventions

Fox/Shackman,Epilogue35Worktoaddresstheseissuesisamatterofpracticalaswellastheoreticalimportance.Someofthemost

common, costly, and intractablemental illnesses—anxiety,depression, schizophrenia, substanceabuse,

autism,andsoon—involveprominentemotionaldisturbances.Collectively, thesepsychiatricdisorders

imposea largerburdenonglobalpublichealthandtheeconomythancancerorcardiovasculardisease

(Collinsetal.,2011;DiLuca&Olesen,2014;Whitefordetal.,2013),underscoringtheneedtodevelopa

deeper understanding of the nature and origins of emotion and themyriadways inwhich emotional

statesandtraitsinfluencethewaywethink,feel,andbehave.

Tothisend,elucidatingthenatureofemotionwillrequirecollaborationamongresearchersdrawnfroma

range of disciplines, which extend far beyond affective psychology and affective neuroscience—from

anthropologists and ethologists to social and cognitive psychologists, from economists to electrical

engineers. Affective science is, by its very nature, interdisciplinary, and to address these fundamental

questions,wewillhavetoworktogether.

We hope that readers of this volume make a lasting impression on our scientific understanding of

emotion,thattheyworktoaddressthe14fundamentalquestionsthatwehaveconsidered,andthatthey

play a role in developing new ones. Ultimately,we hope that a deeper understanding of emotionwill

informandacceleratethedevelopmentofstrategiesforbringingcontentment,compassion,andjoytothe

world.

Fox/Shackman,Epilogue36ACKNOWLEDGEMENTS

This work was supported by the National Institutes of Health (AG051426, AT004952, DA040717,

HD090256,MH018931,MH043454,MH100031,MH107444,MH113347);UniversityofCalifornia,Davis;

California National Primate Research Center; University of Maryland, College Park; Silicon Valley

CommunityFoundation;andseveralgiftstotheCenterforHealthyMinds.Authorsdeclarenoconflictsof

interest.WeappreciatetheassistanceofAndyDeClercq,L.Friedman,andD.Trompandcriticalfeedback

fromL.Pessoa.

AUTHORCONTRIBUTIONS

Theauthorscollectivelydevelopedtheoverallstructureofthereview.A.S.F.andA.J.S.outlinedandwrote

thereview.Alltheauthorsrevisedthereviewandapprovedthefinalversion.

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