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The The subj subjec ecti tive ve expe experi rien ence ce of emotion: a fearful view Joseph E LeDoux1 and Stefan G Hofmann2 We argue that subjective emotional experience, the feeling, is the essence of an of an emotion, and that objective manifestations in behavior and in body or brain physiology are, at best, indirect indicators of these inner experiences. As a result, the most direct way to assess conscious emotional feelings is through verbal self-report. This creates a methodological barrier to studies of conscious feelings in animals. While the behavioral and physiologi physiological cal responses are not ‘emotions,’ they contribute to emotions indirectly, and sometimes profoundly. Whether non-verbal animals have emotional experiences is a difficult, maybe impossible, question to answer in the positive or negati negative. ve. But because behavioral and physiological responses are important contributors to emotions, and the circuits underlying these are highly conserved, studies of animals have an important role in understanding how emotions are expressed and regulated in the brain. Conflation of circuits of circuits that directly give rise to conscious emotional feelings with circuits that indirectly influences these conscious feelings has hampered progress in efforts to understand emotions, and also to understand and to develop treatments for emotional disorders. Recognition of differences of differences in these circuits will allow research in animals to have a lasting impact on understanding of huma human n emotions as research goes forward.
Addresses 1 4 Wash Washin ingt gton on Plac Place, e, Cent Center er for for Neur Neural al Scie Scienc nce, e, New New York York Univ Univer ersi sity ty,, United United States States 2 Depart Departmen mentt of Psycho Psycholog logica icall and Brain Brain Scienc Sciences, es, Boston Boston Unive Universi rsity, ty, United United States States
Corres Correspon pondin ding g author author:: LeDoux LeDoux,, Joseph Joseph E (
[email protected] (
[email protected] )
Curren Currentt Opinio Opinion n in Behavi Behavioral oral Science Sciences s 2018, 19:67–72
This This revi review ew come comes s from from a them themed ed issu issue e on Emotion-cognition interactions Mather and Michael Michael Fanselo Fanselow w Edit Edited ed by Mara Mather
http://dx.doi.org/10.1016/j.cobeha.2017.09.011
2352-1546/ ã 2017 2017 Else Elsevi vier er Ltd. Ltd. All All righ rights ts rese reserv rved ed..
The English word ‘emotion’ is based on the Latin emovere , whic which h means “to move away from.” When first appl applie ied d to psychological events in the 17th century, it pointe pointed d to an excited state of mind of mind that causes movement (behav (behavior ior). ). This This is still the most common meaning of emot em otio ion n in everyday vernacular speech. But in scientific www.sciencedirect.com
discussions, the noun ‘emotion,’ or its adjectival form ‘emotional,’ are variably used to refer to subjective experiences, behavioral movements, physiological responses, and/or cognitions that contribute to any of the abov above. e. Give Given n this multiplicity of referents, it is not surprising that there is debate and confusion about the natu nature re of emotions of emotions [1–11 1–11]. ]. In this this article, we argue that restriction of the use of the term ‘emotion’ ‘emotion’ to subjective experiences, and use of other of other terminology to describe objective responses that are often correlated with emotional experiences would eliminate much much of the of the conceptual confusion. In making this case, we discu iscuss ss several different conceptual approaches to subjective emotional experiences and the brain circuits proposed to underlie such experiences in these approaches approaches.. Because Because the emotion fear has been studied more mo re than than other emotions, especially in relation to brain circuits, and has been the center of much of the controversy ver sy about about the nature of subjectively experienced emotion tion,, we focus on it in our discussion. Because the argument ment made made in this article applies to both fear and anxiety, we will will not distinguish these two terms (for a discussion of the differ differenc ence e see [6]).
Measuri Measuring ng subjec subjectiv tive e experi experienc ences es Before consideri considering ng differen differentt appr approa oach ches es to subjective experiences, it is impo mportant tant to discuss how these unobservable priv privat ate e ev even ents ts are studied. Scientific assessments of inner experiences require some some form of self-reporting self-reporting [12,13 12,13]. ]. Peo People ple can typically give either either a verbal or a nonverba l report of inform informati ation on to which they they have ave introspective acce access ss,, but but cann cannot ot provide a verbal verbal report report of information that that is only processed processed nonconsci conscious ously ly [ 6,14,15 6,14,15]. ]. Fractures Fractures between between conscious conscious and noncon nonconsci scious ous proces processes ses by differ differenc ences es between verbal and non-verb non-verbal al resp respon onse sess have have thus thus play played ed a key key role role in studies of intr intros ospe pect ctiv ive e awar awaren enes esss in huma humans ns.. Whil While e other me meth thod odss of repo report rtin ing g that hat do not not requ equire ire verbal report report have have been been propo proposed sed [ 16–18 16–18], ], these also also depend depend on introspection [15 15]. ]. Verbal self-repor self-reportt remains the the go gold ld standard in studies of cons consci ciou ousn sness ess.. It is most suitable for for asse assess ssiing the content of immediate ex expe perrienc iences es rath rather er than han remembered experiences [14,19 14,19]] and is less useful for assessing the motivation motivationss underlying underlying actions actions since these are often not not cons consci ciou ousl sly y avai availa labl ble e and and ve verb rbal aliz izab able le [20,21 20,21]. ]. Sinc Since e nonnon-ve verb rbal al repo report rtin ing g is the the only only option in non non-ver -verb bal (nonnon-hu huma man) n) orga organi nism sms, s, determining whether other animals have cons consci ciou ous, s, subj subjec ecti tive ve experiences is difficult [6]. Current Current Opinio Opinion n in Behavio Behavioral ral Science Sciences s 2018, 19:1–6
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Cont Contem empo porar rary y view views s of subjective subjective emotional emotional expe experi rien ence ces s in rela relati tion on to brai brain n circ circui uits ts Four contemporary approaches to subjective emotional experiences in the brain, and the historical roots of each, of each, are are desc descri ribe bed d below. Included are approaches in the traditions of Charles Darwin, William James, behaviorism, ism, and and cognitive psychology.
1. The Neuro-Darwinian The Neuro-Darwinian Approach: Subjective Fear Subjective Fear is an Innate State of State of Mind Inherited Inherited from Animal from Animal Ancestors. Ancestors. In his trea treati tise se on huma human n and and animal emotion, Darwin defined emotions as innate “states of mind” that humans have inherited inherited from animal animal ancestors, ancestors, and that, when aroused, cau cause the expression of so-called emotional behaviors [22 22]. ]. This is consistent with the original 17th century use of the f the term emotion mentioned above. It is still the common commonsen sense se view view of emotion that most people have, and and also also underlie Ekman’s widely cited basic emotions theo theory ry [23 23]. ]. A contemporary neuroscience proponent of the tradit tradition ional al Darwinian view is Jaak Panksepp, who views emotions emotions as subjective feelings that emerge from a subcortica subcorticall neural neural circuit that is highly conserved across mammals, mammals, including including humans [24,25 24,25]. ]. The circuit is centere tered d on the amygdala and related subcortical areas [24 24]. ]. In Pank Pankse sepp pp’s ’s formulation, the amygdala circuit, when acti activa vate ted d by a threat to well being, both gives rise to fearful fearful feelings feelings (subjective feelings of fear) and controls innate innate behaviors behaviors and supporting physiological responses that that help help the organism defend against harm. Cognitive elabor elaborati ation on of subcortical of subcortical fear by higher-cortical prefrontal tal circ circui uits ts makes possible introspection and verbal repo report rtss of fear in humans. But the core of fear is the inherited inherited mental mental state arising from the subcortical circuit. Problemati Problematicc for this view is evidence suggesting that the experience of fear is not embodied in the amygdala. Specificall Specifically, y, studies studies in humans show that the amygdala can can resp respon ond d to threats without the person knowing the threat is present and without feeling fear, and other stud studie iess show show that fear can be experienced when the amyg amygda dala la is damaged [26,27 26,27]; ]; for review see [6,7 6,7]. ]. Also Also,, medica medicatio tions ns can change behavioral responses to threats without changing subjective feelings of fear [28,29 28,29]. ]. Thus Thus,, whil while e the amygdala controls behavioral responses to thre threat atss it does not seem to be directly responsible for the subjec subjectiv tive e experience of fear. One could argue that perhap perhapss other other subcortical areas are responsible. But the emphasis in the literature has been on the amygdala. More Mo reov over er,, the the other hypothetical subcortical circuits wou would nee eed d to be identified before the role can be evaluated.
2. The Neuro-Jamesian Approach: Subjective Fear is a Consequence of Feedback of Feedback from Body Responses. William James famously argued that fear and other emotional experiences result by way of feedback from the act of resp respon ondi ding ng [ 30 30]]. Thus, contrary to the commonsense Curren Currentt Opinio Opinion n in Behavi Behavioral oral Science Sciences s 2018, 19:1–6
view, fear does not cause the responses but instead results as a consequence of the responses. Modern versions of this this theo theory ry by Antonio Damasio [31,32 31,32]] and A.D. Craig [33,34 33,34]] have proposed that fearful and other emotional feelin fee lings gs are the result of activity in body sensing circuits in the the neocortex (somato-sensory and/or insula areas) that repr repres esen entt body body states, such as those triggered when thre threat atss acti activa vate te amygdala circuits. Initially, Damasio emphasized cortical body sensing circuits but more recently has emphasized brainstem circuits [32 32]. ]. As in Panksepp’s theory, cognitive elaboration by highercortic cortical al circui circuits ts allows introspection and self-reporting about these states in Damasio’s theory. While these circ circui uits ts clear clearly ly represent body states, convincing evidenc dence e that that these representations are the main causes of emotional experiences is lacking [6]. We propose below that that body ody feedback makes important contributions to emotional experiences, but as modulators rather than as dire direct ct causes.
3. The Neuro-Behaviorist Neuro-Behaviorist Approach: Approach: Subjective Fear is Fear is a Folk Psychological Construct that Should be Replaced be Replaced by a Scie Scienntific Explana Explanatio tion. n. In the early 20th century, behaviorists eliminated mental states from the causal chain between external external stimuli stimuli and behavioral responses. However, they retained retained mental mental state terms when describing the empirical relati relation on between stimuli and responses. For example, ‘fea ‘fearr’ was was used to characterize the relation between thre threat atss and and defensive behaviors [35 35]. ]. With the rise of physiological approaches to behavior in the middle of the of the 20th 20th cent centur ury, y, fear became a hypothetical physiological state (central (central state), that connects threats with defensive behaviors [36 36]. ]. The intended purpose of this approach was to satisfy the behaviorist constraint against using subjec subjectiv tive e explan explanati ations ons of behavior. Ultimately, the amygdala emerged as the locus of the central fear state [37,38 37,38]]. The central state model has been popular in behavioral neuroscience [39–42 39–42]. ]. Many who call upon the the cent centra rall state view today are ambivalent abo about the ext extent ent to which fear means subjective fear or a nonsubjective state. But adherents of a strong version of the the posi positi tion on argue that subjective, conscious fear is an inaccurate inaccurate scientific scientific construct that can be replaced with a more rigorous rigorous scientific notion of fear of fear as a non-subjective stat state e of the amygdala-centered circuits [42 42]. ]. The wellknow known n lack lack of correlation between verbal reports and amygdala amygdala activity activity in humans [43–45 43–45]] is, in this view view,, due due to the lack of acce access ss to amygdala activity by cognitivebased based intros introspec pectio tion, n, and hence verbal report. In short, verbal ver bal report report of subjective experience is viewed as a less desi desira rabl ble e way way of asse assessi ssing ng fear than simply measuring amygdala-controlled responses. The mechanisti mechanisticc reason a threat elicits defense responses is beca becaus use e it activates cells and synapses in circuits that control control those responses. The fear construct is superfluous in this context [6,7,28,46 6,7,28,46]. ]. It adds conceptual baggage www.sciencedirect.com
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that reifies fear and imbues the circuit with the exact phenomenological properties that are trying to be avoided [47 47]. ]. The way to avoid these problems is by using nonsubjective terminology to name the non-subjective central tral stat states es.. Such states, for example, can be referred in terms of neural activity in a defe defens nsiv ive e survival circuit (rathe (ratherr than than in a fear circuit) [4]. This solves part of the problem but leaves open the question of how conscious fear comes about. The neuro-cognitive approach addres addresses ses this this issue.
4. The Neuro-Cognitive Approach: Neuro-Cognitive Approach: Subjective Fear Fear Emerges Emerges from Higher-Order Processing. Cognitive approaches to emotio emo tion n arose arose in the 1960s in an effort to address certain critic criticisms isms of the of the Jamesian Jamesian approach, and to overcome the behavioris behaviorist’s t’s restricti restrictions ons on inner explanations. Stanley Schach Schachter ter propos proposed ed that emotional experiences result when we interpret physiological arousal in the brain and/or body in light of cognitive assessments of social situations situations,, allowing allowing the categorization and labeling of the of the experience [48,49 48,49]. ]. While there have been a number of cognitive cognitive approaches approaches to emotion [50–53 50–53], ], recent theorizing ing has has emphasized that emotional experiences are cognitive nitive construct constructions ions based on conceptualizations of situasituation tionss [11,54–56 11,54–56]] or higher-order states that emerge as a resu result lt of the of the cognitive integration in working memory of diverse diverse sources sources of inform informati ation on from within the brain and body body [6,7,37,57,58 6,7,37,57,58]. ]. Both Both of these of these positions reject the idea that emotional emotional experiences arise from subcortical circuits (views of the Neuro-Darwinian and Neuro-Jamesian approa approache ches) s) and also reject the idea that the subjective experience is a non-scientific construct (Neuro-Behaviorist approa approach) ch).. The higher-order approach builds on recent developmen me nts in the science and philosophy of consciousness (e.g (e.g.. [7,59–61 7,59–61]), ]), arguin arguing g that a general general network network of cognitions tions underl underlies ies both cognitive and emotional states of consciousne consciousness. ss. In higher-order emotion theory, what distinguishes tinguishes cognitive cognitive and emotional states of consciousness, ness, and different kinds of emotional of emotional states, is the kind of inputs inputs processed. processed. The subcortical fear circuit of the the other models models become becomess a defens defensive ive survival circuit that detects and respon responds ds to threats. The consequences of defensive surviv survival al circui circuitt activation (brain arousal, body feedback, etc.) contribut contribute e indirectly to the experience of fear of fear but do not determ determine ine it. Fear is the cognitive assessment that yo you u are are in harms way, a view that allows fear to arise from activi activity ty in any survival circuits (fear of being harmed by starvation, dehydration, hypothermia, reproductive isolation, tion, and so forth) forth),, or by existential concerns (such as fear of the the eventuality of death of death or the meaninglessness of your of your life life), ), in addition to predatory-related dangers that trigger the defens defensive ive survival circuit.
5: Summar Summaryy of the the Four Four Approaches. Approaches. The neuro-Darwinian, neur neuroo-Ja Jame mesia sian, n, and and neuro-behaviorist approaches all www.sciencedirect.com
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imply that if through psychotherapy or pharmaceutical treatm treatment ent you successfully reduce amygdala activity, as measured by amygdala-mediated behavioral and/or physiological iological responses, responses, pathological fear should be ameliorate rated. d. But But different reasons underlie this conclusion in each each approa approach. ch. In the neuro-Darwinian approach, treatments that weaken defensive behavior should treat fear prob proble lems ms by altering amygdala activity underlying both beha behavi vior or and and feelings. In the neuro-Jamesian approach, treatments that weaken defensive behavior by altering amygdala amygdala activity activity should treat fear problems because the behaviors, being weaker, shou should ld give give rise to less body feedback and thus weaker subjective feelings. In the neuro-behaviorist approach, altering amygdala activity through behavioral (CBT) or pharmaceutical treatments should should treat treat pathological fear because the problems are due to the non-subjective amygdala state. Once this changes, changes, subjective subjective fear might also change because it is an indire indirect ct cognitive readout of amygdala activity. However, whether whether self-reported feelings change is less important tant than than whether defensive behavior changes since the latt latter er is a direc irectt readout of amygdala activity. A major chal challe leng nge e for for these approaches is accounting for the fail failur ure e of studies using defensive behaviors in animals as me mean anss of drug-discovery of drug-discovery to generate novel agents with clinic clinical al efficac efficacy y in treating fear and anxiety [6,28,29,62 6,28,29,62]. ].
Cons Consci ciou ous s feel feelin ings gs in clin clinic ical al asse assess ssmen mentt A major reason why people seek the help of mental of mental health spec specia iali list stss is because they feel bad and want to feel better. A treatment that reduces behavior (freezing, behavioral timidity, avoidance) and physiology (hyperarou arousa sal) l) but but does not diminish subjectively reported fearful feelings is not likely likely to be viewed as a satisfactory outc outcom ome e by the afflict afflicted ed person person.. In the contemporary cognitive therapy literature, selfreport reports, s, and the subjective experiences that these reports reflect, reflect, have not been given much credence. This reflects the influen influence ce of behaviorism of behaviorism in the development of both of both traditiona traditionall behavioral behavioral therapy [63 63]] and cognitive behavioral ioral therap therapy y (CBT) [64 64], ], as well as findings suggesting that behaviora behaviorall physiological responses related to fear or anxiety in humans are poorly correlated [43–45 43–45]. ]. A recent argu argume ment nt has has been made for more attention to verbal repo report rtss of subjective of subjective experiences, but mainly to validate non-subjective measures [65 65]. ]. This reflects the dominanc nance e of the of the amygdala fear center view described above in clinic clinical al concep concepts. ts. If behavioral, physiological and sub jective responses are all products of the of the same circuit, one resp respon onse se is as good as another as a way to judge clinical outcome. outcome. This logi logicc is also apparent in the NIHM RDoC initiative, which treats subjective reports as just another meas me asur ure e of fear. Kozak and Cuthbert [66 66], ], for example, note note that that “ . . . the RDoC approach accords self-report data data no special precedence among different measurement Current Current Opinio Opinion n in Behavio Behavioral ral Science Sciences s 2018, 19:1–6
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classes, any of which might contribute to a nomolo nomologic gical al net net (p. 292).” An important important advantag advantage e of the of the neuro-cognitive neuro-cognitive approach to fear fear is that it accoun accounts ts for the two troubling observation tionss me ment ntio ione ned d abov above e that are not not easi easily ly hand andled led by fearfear-cen cente terr views: views: subjec subjectiv tive e fear fear does not not requ requir ire e the the amygda amygdala, la, and medica medicati tions ons that that target the amygd amygdala ala do not neces necessar sarily ily reliev relieve e subjec subjecti tive ve fear. fear. It would seem that that the neuro-cognitive approach should mesh mesh well well with with modern CBT. CBT. Howeve However, r, despi despite te the centra centrali lity ty of introspection and and cogn cognit itiv ive e proc proces esse sess in human human mental mental life, as noted above, above, subjecti subjective ve report report never reached a central stat status us in CBT. Self-repo Self-report rt has always been seen as an easy but unreliable way to measure anxiety and fear. For example, Zoellner and Foa [67 67]] agree with Kozak and Cuthbert that self-r self-repo eports rts do not have any special status, noting that “self-report is one piece of the of the net in terms of studying of studying a phenomenon.” But they nevertheless go on to say that self-repor self-reports ts “should “should be considered potential valid measur sures of key of key constructs, some of which cannot be measure sured d in any other way, and sometimes the best measure of the construct of intere interest st (p. 334).” Toda Today, y, CBT CBT therapists routinely use subjective patient repo report rt as part of treatment. However, its value continues to be debated. Some argue that self-reported fear is an inad inadeq equa uate te me meas asur ure e of the patient’s emotional state because because reduction reduction in reported fear during exposure sessions sions does does not predict long-term treatment effects [68,69 68,69]. ]. While While this finding is consistent with the neuro-behaviorist (non-subjective) amygdala fear state model described abov above, e, the the evidence presented is not especially strong, and and othe otherr findings directly contradict the conclusion. Specifically, more recent clinical trials examining the augmen augmentat tation ion effect effect of D-cycloserine (DCS), a partial ago agonist nist at the glycine recognition site of the NMDA recept receptor or comple complex, x, show the DCS enhances exposure therap therapy y primar primarily ily in those people who report a clear reduction of reported fear during the exposures [70,71 70,71]. ]. This This sugges suggests ts that the reduction in reported fear ratings during during an exposure session is, in fact, a cruc crucia iall factor that determines determines the success of treatment of treatment [72 72]. ]. Also intriguing is the recent finding that Pavlovian conditioned threat resp respon onses ses can can be extinguished without the arousal of consci conscious ous fear fear [73 73]. ]. We argue that subjective reports of fear and anxiety are not not unre unreli liab able le proxy measures of fear and anxiety, as sugges suggested ted by the neuro-behaviorist model. Rather, they are are the the best direct, and, at least so far, the only measures easily easily accessi accessible ble for clinicians to assess the efficacy of treatm treatment ent.. If this is correct, therapists need to carefully list listen en to the clients’ report about their emotional states, furt furthe herr deve develo lop p reliable assessment instruments of Curren Currentt Opinio Opinion n in Behavi Behavioral oral Science Sciences s 2018, 19:1–6
subjective reports, and utilize verbal strategies to elicit and modify modify them. However, we suggest that this be done afte afterr othe otherr approaches, such as CBT or pharamceutical treatm treatment ents, s, to first dampen the amygdala central state, which which indire indirectl ctly y affects subjective experience. We also recommend recommend that future research re-examine the relationship ship betw betwee een n subjective report, behaviors, and physiologica logicall respon responses ses of fear and anxiety in order to explain the reason reasonss for the dissociation between these measures.
Confl Conflic ictt of inte intere rest st stat statem emen entt Nothing declared.
Funding Funded in part by the James S. McDonnell Foundation 21 Century Science Initiative in Understanding Human Cogn Cognit itio ion n – Spec Specia iall Initiative. st
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