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The Subjective Experience of Emotion A Fearful View

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The subjective experience of emotion: a fearful view


Joseph E LeDoux1 and Stefan G Hofmann2

We argue that subjective emotional experience, the feeling, is discussions, the noun ‘emotion,’ or its adjectival form
the essence of an emotion, and that objective manifestations in ‘emotional,’ are variably used to refer to subjective
behavior and in body or brain physiology are, at best, indirect experiences, behavioral movements, physiological re-
indicators of these inner experiences. As a result, the most sponses, and/or cognitions that contribute to any of the
direct way to assess conscious emotional feelings is through above. Given this multiplicity of referents, it is not
verbal self-report. This creates a methodological barrier to surprising that there is debate and confusion about the
studies of conscious feelings in animals. While the behavioral nature of emotions [1–11].
and physiological responses are not ‘emotions,’ they
contribute to emotions indirectly, and sometimes profoundly. In this article, we argue that restriction of the use of the
Whether non-verbal animals have emotional experiences is a term ‘emotion’ to subjective experiences, and use of other
difficult, maybe impossible, question to answer in the positive terminology to describe objective responses that are often
or negative. But because behavioral and physiological correlated with emotional experiences would eliminate
responses are important contributors to emotions, and the much of the conceptual confusion. In making this case,
circuits underlying these are highly conserved, studies of we discuss several different conceptual approaches to
animals have an important role in understanding how emotions subjective emotional experiences and the brain circuits
are expressed and regulated in the brain. Conflation of circuits proposed to underlie such experiences in these
that directly give rise to conscious emotional feelings with approaches. Because the emotion fear has been studied
circuits that indirectly influences these conscious feelings has more than other emotions, especially in relation to brain
hampered progress in efforts to understand emotions, and also circuits, and has been the center of much of the contro-
to understand and to develop treatments for emotional versy about the nature of subjectively experienced emo-
disorders. Recognition of differences in these circuits will allow tion, we focus on it in our discussion. Because the argu-
research in animals to have a lasting impact on understanding ment made in this article applies to both fear and anxiety,
of human emotions as research goes forward. we will not distinguish these two terms (for a discussion of
the difference see [6]).
Addresses
1
4 Washington Place, Center for Neural Science, New York University, Measuring subjective experiences
United States Before considering different approaches to subjective
2
Department of Psychological and Brain Sciences, Boston University, experiences, it is important to discuss how these
United States
unobservable private events are studied. Scientific
Corresponding author: LeDoux, Joseph E ([email protected]) assessments of inner experiences require some form
of self-reporting [12,13]. People can typically give either
a verbal or a nonverbal report of information to which
Current Opinion in Behavioral Sciences 2018, 19:67–72 they have introspective access, but cannot provide a
This review comes from a themed issue on Emotion-cognition verbal report of information that is only processed non-
interactions consciously [6,14,15]. Fractures between conscious and
Edited by Mara Mather and Michael Fanselow nonconscious processes by differences between verbal
and non-verbal responses have thus played a key role in
studies of introspective awareness in humans. While
other methods of reporting that do not require verbal
http://dx.doi.org/10.1016/j.cobeha.2017.09.011 report have been proposed [16–18], these also depend on
2352-1546/ã 2017 Elsevier Ltd. All rights reserved. introspection [15].

Verbal self-report remains the gold standard in studies


of consciousness. It is most suitable for assessing
the content of immediate experiences rather than
remembered experiences [14,19] and is less useful for
The English word ‘emotion’ is based on the Latin assessing the motivations underlying actions since these
emovere, which means “to move away from.” When first are often not consciously available and verbalizable
applied to psychological events in the 17th century, it [20,21]. Since non-verbal reporting is the only option
pointed to an excited state of mind that causes movement in non-verbal (non-human) organisms, determining
(behavior). This is still the most common meaning of whether other animals have conscious, subjective
emotion in everyday vernacular speech. But in scientific experiences is difficult [6].

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2 Emotion-cognition interactions

Contemporary views of subjective emotional view, fear does not cause the responses but instead results
experiences in relation to brain circuits as a consequence of the responses. Modern versions of
Four contemporary approaches to subjective emotional this theory by Antonio Damasio [31,32] and A.D. Craig
experiences in the brain, and the historical roots of each, [33,34] have proposed that fearful and other emotional
are described below. Included are approaches in the feelings are the result of activity in body sensing circuits
traditions of Charles Darwin, William James, behavior- in the neocortex (somato-sensory and/or insula areas) that
ism, and cognitive psychology. represent body states, such as those triggered when
threats activate amygdala circuits. Initially, Damasio
1. The Neuro-Darwinian Approach: Subjective Fear is an emphasized cortical body sensing circuits but more
Innate State of Mind Inherited from Animal Ancestors. In his recently has emphasized brainstem circuits [32]. As in
treatise on human and animal emotion, Darwin defined Panksepp’s theory, cognitive elaboration by higher-
emotions as innate “states of mind” that humans have cortical circuits allows introspection and self-reporting
inherited from animal ancestors, and that, when aroused, about these states in Damasio’s theory. While these
cause the expression of so-called emotional behaviors circuits clearly represent body states, convincing evi-
[22]. This is consistent with the original 17th century dence that these representations are the main causes of
use of the term emotion mentioned above. It is still the emotional experiences is lacking [6]. We propose below
commonsense view of emotion that most people have, that body feedback makes important contributions to
and also underlie Ekman’s widely cited basic emotions emotional experiences, but as modulators rather than
theory [23]. A contemporary neuroscience proponent of as direct causes.
the traditional Darwinian view is Jaak Panksepp, who
views emotions as subjective feelings that emerge from a 3. The Neuro-Behaviorist Approach: Subjective Fear is a Folk
subcortical neural circuit that is highly conserved across Psychological Construct that Should be Replaced by a Scien-
mammals, including humans [24,25]. The circuit is cen- tific Explanation. In the early 20th century, behaviorists
tered on the amygdala and related subcortical areas [24]. eliminated mental states from the causal chain between
In Panksepp’s formulation, the amygdala circuit, when external stimuli and behavioral responses. However, they
activated by a threat to well being, both gives rise to retained mental state terms when describing the empiri-
fearful feelings (subjective feelings of fear) and controls cal relation between stimuli and responses. For example,
innate behaviors and supporting physiological responses ‘fear’ was used to characterize the relation between
that help the organism defend against harm. Cognitive threats and defensive behaviors [35]. With the rise of
elaboration of subcortical fear by higher-cortical prefron- physiological approaches to behavior in the middle of the
tal circuits makes possible introspection and verbal 20th century, fear became a hypothetical physiological
reports of fear in humans. But the core of fear is the state (central state), that connects threats with defensive
inherited mental state arising from the subcortical circuit. behaviors [36]. The intended purpose of this approach
was to satisfy the behaviorist constraint against using
Problematic for this view is evidence suggesting that the subjective explanations of behavior. Ultimately, the
experience of fear is not embodied in the amygdala. amygdala emerged as the locus of the central fear state
Specifically, studies in humans show that the amygdala [37,38]. The central state model has been popular in
can respond to threats without the person knowing the behavioral neuroscience [39–42]. Many who call upon
threat is present and without feeling fear, and other the central state view today are ambivalent about the
studies show that fear can be experienced when the extent to which fear means subjective fear or a non-
amygdala is damaged [26,27]; for review see [6,7]. Also, subjective state. But adherents of a strong version of
medications can change behavioral responses to threats the position argue that subjective, conscious fear is an
without changing subjective feelings of fear [28,29]. inaccurate scientific construct that can be replaced with a
Thus, while the amygdala controls behavioral responses more rigorous scientific notion of fear as a non-subjective
to threats it does not seem to be directly responsible for state of the amygdala-centered circuits [42]. The well-
the subjective experience of fear. One could argue that known lack of correlation between verbal reports and
perhaps other subcortical areas are responsible. But the amygdala activity in humans [43–45] is, in this view, due
emphasis in the literature has been on the amygdala. to the lack of access to amygdala activity by cognitive-
Moreover, the other hypothetical subcortical circuits based introspection, and hence verbal report. In short,
would need to be identified before the role can be verbal report of subjective experience is viewed as a less
evaluated. desirable way of assessing fear than simply measuring
amygdala-controlled responses.
2. The Neuro-Jamesian Approach: Subjective Fear is a
Consequence of Feedback from Body Responses. William The mechanistic reason a threat elicits defense responses
James famously argued that fear and other emotional is because it activates cells and synapses in circuits that
experiences result by way of feedback from the act of control those responses. The fear construct is superfluous
responding [30]. Thus, contrary to the commonsense in this context [6,7,28,46]. It adds conceptual baggage

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Conscious emotion LeDoux and Hofmann 3

that reifies fear and imbues the circuit with the exact imply that if through psychotherapy or pharmaceutical
phenomenological properties that are trying to be avoided treatment you successfully reduce amygdala activity, as
[47]. The way to avoid these problems is by using non- measured by amygdala-mediated behavioral and/or phys-
subjective terminology to name the non-subjective cen- iological responses, pathological fear should be amelio-
tral states. Such states, for example, can be referred in rated. But different reasons underlie this conclusion in
terms of neural activity in a defensive survival circuit each approach. In the neuro-Darwinian approach, treat-
(rather than in a fear circuit) [4]. This solves part of the ments that weaken defensive behavior should treat fear
problem but leaves open the question of how conscious problems by altering amygdala activity underlying both
fear comes about. The neuro-cognitive approach behavior and feelings. In the neuro-Jamesian approach,
addresses this issue. treatments that weaken defensive behavior by altering
amygdala activity should treat fear problems because the
4. The Neuro-Cognitive Approach: Subjective Fear Emerges behaviors, being weaker, should give rise to less body
from Higher-Order Processing. Cognitive approaches to feedback and thus weaker subjective feelings. In the
emotion arose in the 1960s in an effort to address certain neuro-behaviorist approach, altering amygdala activity
criticisms of the Jamesian approach, and to overcome the through behavioral (CBT) or pharmaceutical treatments
behaviorist’s restrictions on inner explanations. Stanley should treat pathological fear because the problems are
Schachter proposed that emotional experiences result due to the non-subjective amygdala state. Once this
when we interpret physiological arousal in the brain changes, subjective fear might also change because it is
and/or body in light of cognitive assessments of social an indirect cognitive readout of amygdala activity. How-
situations, allowing the categorization and labeling of the ever, whether self-reported feelings change is less impor-
experience [48,49]. While there have been a number of tant than whether defensive behavior changes since the
cognitive approaches to emotion [50–53], recent theoriz- latter is a direct readout of amygdala activity. A major
ing has emphasized that emotional experiences are cog- challenge for these approaches is accounting for the
nitive constructions based on conceptualizations of situa- failure of studies using defensive behaviors in animals
tions [11,54–56] or higher-order states that emerge as a as means of drug-discovery to generate novel agents with
result of the cognitive integration in working memory of clinical efficacy in treating fear and anxiety [6,28,29,62].
diverse sources of information from within the brain and
body [6,7,37,57,58]. Both of these positions reject the idea
that emotional experiences arise from subcortical circuits Conscious feelings in clinical assessment
(views of the Neuro-Darwinian and Neuro-Jamesian A major reason why people seek the help of mental health
approaches) and also reject the idea that the subjective specialists is because they feel bad and want to feel
experience is a non-scientific construct (Neuro-Behavior- better. A treatment that reduces behavior (freezing,
ist approach). behavioral timidity, avoidance) and physiology (hyper-
arousal) but does not diminish subjectively reported
The higher-order approach builds on recent develop- fearful feelings is not likely to be viewed as a satisfactory
ments in the science and philosophy of consciousness outcome by the afflicted person.
(e.g. [7,59–61]), arguing that a general network of cogni-
tions underlies both cognitive and emotional states of In the contemporary cognitive therapy literature, self-
consciousness. In higher-order emotion theory, what dis- reports, and the subjective experiences that these reports
tinguishes cognitive and emotional states of conscious- reflect, have not been given much credence. This reflects
ness, and different kinds of emotional states, is the kind of the influence of behaviorism in the development of both
inputs processed. The subcortical fear circuit of the other traditional behavioral therapy [63] and cognitive behav-
models becomes a defensive survival circuit that detects ioral therapy (CBT) [64], as well as findings suggesting
and responds to threats. The consequences of defensive that behavioral physiological responses related to fear or
survival circuit activation (brain arousal, body feedback, anxiety in humans are poorly correlated [43–45]. A recent
etc.) contribute indirectly to the experience of fear but do argument has been made for more attention to verbal
not determine it. Fear is the cognitive assessment that reports of subjective experiences, but mainly to validate
you are in harms way, a view that allows fear to arise from non-subjective measures [65]. This reflects the domi-
activity in any survival circuits (fear of being harmed by nance of the amygdala fear center view described above
starvation, dehydration, hypothermia, reproductive isola- in clinical concepts. If behavioral, physiological and sub-
tion, and so forth), or by existential concerns (such as fear jective responses are all products of the same circuit, one
of the eventuality of death or the meaninglessness of your response is as good as another as a way to judge clinical
life), in addition to predatory-related dangers that trigger outcome. This logic is also apparent in the NIHM RDoC
the defensive survival circuit. initiative, which treats subjective reports as just another
measure of fear. Kozak and Cuthbert [66], for example,
5: Summary of the Four Approaches. The neuro-Darwinian, note that “ . . . the RDoC approach accords self-report
neuro-Jamesian, and neuro-behaviorist approaches all data no special precedence among different measurement

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4 Emotion-cognition interactions

classes, any of which might contribute to a nomological subjective reports, and utilize verbal strategies to elicit
net (p. 292).” and modify them. However, we suggest that this be done
after other approaches, such as CBT or pharamceutical
An important advantage of the neuro-cognitive approach treatments, to first dampen the amygdala central state,
to fear is that it accounts for the two troubling observa- which indirectly affects subjective experience. We also
tions mentioned above that are not easily handled by recommend that future research re-examine the relation-
fear-center views: subjective fear does not require the ship between subjective report, behaviors, and physio-
amygdala, and medications that target the amygdala do logical responses of fear and anxiety in order to explain
not necessarily relieve subjective fear. It would seem the reasons for the dissociation between these measures.
that the neuro-cognitive approach should mesh well with
modern CBT. However, despite the centrality of intro-
spection and cognitive processes in human mental life, Conflict of interest statement
as noted above, subjective report never reached a central Nothing declared.
status in CBT.

Self-report has always been seen as an easy but unreliable Funding


way to measure anxiety and fear. For example, Zoellner Funded in part by the James S. McDonnell Foundation
and Foa [67] agree with Kozak and Cuthbert that 21st Century Science Initiative in Understanding Human
self-reports do not have any special status, noting that Cognition – Special Initiative.
“self-report is one piece of the net in terms of studying a
phenomenon.” But they nevertheless go on to say that
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