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A Neuroscientist's Perspective on Debates about the Nature of Emotion

Joseph LeDoux
Emotion Review 2012 4: 375
DOI: 10.1177/1754073912445822
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Comment

A Neuroscientists Perspective on Debates

about the Nature of Emotion

Emotion Review
Vol. 4, No. 4 (October 2012) 375379
The Author(s) 2012
ISSN 1754-0739
DOI: 10.1177/1754073912445822
er.sagepub.com

Joseph LeDoux

Center for Neural Science, New York University, USA

Nathan Kline Institute, Orangeburg, USA

Abstract
The target articles by Dixon (2012), Scarantino (2012), and Mulligan and
Scherer (2012) explore the nature of emotion from philosophical and
psychological perspectives. I discuss how neuroscience can also contribute
to debates about the nature of emotion. I focus on the aspects of emotion
that usually fall within the topic of basic emotions, but conclude that we
may need to revise how we conceive and study these kinds of emotional
states in relation to the brain.

Keywords
amygdala, brain, emotion, explicit memory, fear, hippocampus, implicit
memory, memory, mind, psychiatry, unconscious, working memory

In this comment I evaluate three major approaches to the emotional brain and relate these to the target articles by Dixon (2012),
Scarantino (2012), and Mulligan and Scherer (2012). The first
approach assumes that the brain has a single emotion system that
is responsible for the various processes related to emotions. The
second assumes that so-called basic emotions constitute a set of
biologically defined emotions, each mediated by a distinct brain
circuit. The third approach focuses on one emotion at a time,
attempting to understand canonical instances of emotion, and
makes no particular assumption about the relation of the brain systems involved in different emotions. The latter may be the least
satisfying in terms of offering an immediate, all-encompassing
theory of emotion, but in the long run might provide a basis for an
approach to emotion centered on brain circuits.

One System for All Emotions: The Limbic

System Concept
In the middle of the 20th century, neuroscientist Paul MacLean
attempted to provide an all-encompassing theory of the
emotional brain (MacLean, 1949, 1952, 1970). Drawing on the

anatomical wisdom of the day, MacLean situated emotion in

areas of the medial (presumed older) cortex (e.g., hippocampus,
cingulate gyrus) and cognition in the lateral (presumed newer)
cortex. The medial cortex and related subcortical forebrain
areas were said to form the paleomammalian brain, which
contrasted with the later emerging cortex, which MacLean
called the neomammalian brain (also known as the neocortex).
Both the limbic system and neocortex were viewed as novel
forebrain structures present in mammals but not in other
vertebrates, and that were layered on top of the reptilian brain
(the basal ganglia and brainstem). According to MacLean,
specific emotions (specific feelings like fear, love, and anger)
are products of the limbic system, whereas cognitive functions
(thought and language) are functions of the neocortex.
MacLeans ideas of old and new cortex were based on the
anatomical wisdom of the day. But this anatomical foundation
of the limbic system theory has been discredited by modern
comparative neurobiology, which has shown that the two
regions that MacLean argued were novel mammalian structures
both have precursors in reptiles and birds (Butler & Hodos,
2005; Nauta & Karten, 1970; Northcutt & Kaas, 1995; Swanson,
1983). Further, MacLeans notion that the architecture of
paleomammalian (limbic) cortical areas is ill-suited to cognition,
and is instead ideal for irrational emotions, is also unfounded.
The hippocampus, which MacLean thought of as the centerpiece
of the limbic system, emerged as being essential for important
cognitive functions, such as declarative memory (Eichenbaum,
2004; Squire & Kandel, 1999) and spatial mapping of the
environment (OKeefe & Nadel, 1978). Finally, there is little
evidence that areas identified as components of the limbic
system function as a unified emotion system (see Kotter &
Meyer, 1992; LeDoux, 1987, 1996).
Still, the idea that there might be circuits in the mammalian
brain that are relatively specialized for functions typically referred
to as emotional and are conserved to some extent throughout
mammals, including humans, continues to be relevant. The
question is, how should we account for these functions?

Corresponding author: Joseph LeDoux, Center for Neural Science, NYU Emotional Brain Institute, NYU and Nathan Kline Institute, 4 Washington Place, New York, NY 10011,
USA. Email: ledoux@cns.nyu.edu

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376 Emotion Review Vol. 4 No. 4

Different Systems for Different Emotions:

Basic Emotions in the Brain
Basic emotions theory argues that certain emotions are hardwired in the brain, are expressed the same and recognized
universally around the world, are part of human nature, and are
conserved to some extent across mammalian species (Damasio,
1994, 1999; Ekman, 1999; Izard, 2007; Panksepp, 1998, 2005;
Tomkins, 1962). Although the emotions listed by different
authors as basic emotions differ somewhat (Ortony & Turner,
1990), the fundamental idea is that human feelings, defined by
introspective experience and labeled with common language
emotion words (usually English words), reflect evolutionarily
conserved circuits (affect programs).
Some neuroscientists have attempted to identify brain areas
and circuits that account for basic emotions. Panksepp has the best
developed brain-based basic emotions theory (e.g., Panksepp,
1998, 2005). He argues that the way to capture innate basic
emotions in their pure form is when they are aroused artificially by
direct stimulation of brain areas where those operating systems are
most concentrated. On the basis of such results Panksepp proposed
separate circuits involved in seven basic emotions: seeking, fear,
rage, lust, care, panic, and play. Each circuit controls specific
emotional behaviors (e.g., the fear circuit controls defensive
behavior, the lust circuit sexual behavior) and is also responsible
for specific feelings (e.g., fear, lust, anger). The relation of innate
conserved circuits to feelings is particularly important for
Panksepp, who notes that affective consciousness is an intrinsic
function of the brain, shared homologously by all mammalian
species (Panksepp, 2005, p. 30). Although his basic emotions are
not the same as those in most psychological theories, as noted
before, psychological theories do not have all the same categories
either.
Thus, for Panksepp, the existence of conserved circuits for
emotional behavior means that feelings too are conserved across
mammals. However, evidence that these circuits are responsible
for the behaviors proposed relies on results from electrical brain
stimulation, a method that is problematic since it indiscriminately
activates both neurons and axons in an area and, among other
things, cannot be used to precisely identify the areas responsible
for the behaviors that result. But this is not the main problem.
Regardless of the validity of the conclusions for the relation of
the circuits proposed to emotional behavior (some of which may
be valid and some not), there is no direct evidence that these
circuits contribute to conscious feelings in animals (how could
there be?). As indirect evidence, Panksepp cites findings from
studies in which electrical stimulation has been delivered to
brain areas in humans (supposedly the same brain areas that are
responsible for basic emotional behavior in animals). However,
such methods are also highly problematic when applied to the
human brain (even more problematic than in animals since they
are necessarily cruder in human studies, and are only used as
part of diagnosis/treatment in patients with pathological brains).
For a review of the problems involved in using electrical
stimulation findings to reveal circuits dedicated to specific basic

emotions and their corresponding feelings in the human brain,

see Barrett et al. (2007).
At the same time, we also need to be careful not to go too far
and reject the idea that there are specific circuits of emotional
behavior. For example, Barrett argues that the lack of emotion
specificity in fMRI findings showing activations to emotional
stimuli (usually faces) challenges the idea that there is emotion
specificity in the brain (Barrett, 2006). There are two responses
to this critique. First, it is not at all clear that emotional face
stimuli are the most appropriate stimuli for studying highly
conserved neural circuits. Second, behavioral functions are
localized not at the level of brain areas, which is the level of
resolution fMRI can reveal, but at the level of microcirucits
within brain areas.
Thus, while I disagree with Panksepp about some (though
not all) of the details of the specific circuits involved in
emotional behavior (on methodological grounds), and especially
disagree about the relation of circuits in rodents to human
feelings (on methodological and philosophical grounds), I share
with Panksepp the conviction that there are innate emotion
circuits that are conserved in mammals, including humans.

One Emotion at a Time

Most neuroscientists today who explore brain functions related
to emotion in animals tend to be more interested in circuits that
contribute to individual kinds of emotional states, as measured
within specific kinds of well-controlled behavioral tasks, than in
simultaneously accounting for many emotions (i.e., all basic
emotions, however defined). For example, some researchers
focus on fear, others on aggression, others on reward, and so on.
For each such behavioral category, progress is being made in
exploring the contribution not so much of gross brain areas as of
systems of microcircuits, each consisting of specific neurons
interconnected by specific synapses and with communication
within and between such neurons identified in terms of specific
molecules regulated by genetic and epigenetic factors.
When I wrote The Emotional Brain (LeDoux, 1996), I
emphasized work on fear. I did this primarily because there was
and still is no clear definition of emotion, as the present target
articles demonstrate. I therefore decided to focus on one emotion
that there was good agreement about (most theories accept fear
as an emotion), and that I happened to have researched quite a
bit. The basic idea was that such a focus would allow progress
on a well-defined aspect of emotion, even if it failed to solve the
problem of emotion in general.
But what do I mean when I say I study fear in animals.
There are two important things to note. First, I am not studying
fear in the general sense. I am studying those aspects of fear
that can be modeled by Pavlovian defense (fear) conditioning, a
procedure in which an emotionally neutral stimulus comes to
elicit defense responses (freezing and supporting physiological
changes mediated by the autonomic nervous system and the
endocrine system) (e.g., Johansen, Cain, Ostroff, & LeDoux,
2011; LeDoux, 2000, 2008; Maren, 2005). This may seem to be

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LeDoux A Neuroscientists Perspective on Emotion 377

a very narrow focus, but in fact it is a pretty good model of how

specific stimuli, through experience, acquire threat value and
come to elicit defensive responses. It also seems to be relevant
to some psychiatric conditions such as specific phobic and posttraumatic stress disorder (PTSD) (Bouton, Mineka, & Barlow,
2001; Grillon, Southwick, & Charney, 1996; Shalev, RagelFuchs, & Pitman, 1992). Second, I am not studying fear in the
sense of feelings or affective consciousness. I am studying how
the brain detects and responds to threats (LeDoux, 2008).
Fear conditioning is a good example of a task that has been
used to explore one aspect of one emotion with the exquisite
tools available in modern neuroscience. Some of the findings
will be described in what follows.

of coordination across components of a broad system. However,

given my critique of the limbic system concept before, I think it
would be best to look for other, more grounded mechanisms.
The basic emotions approach might work since, in their model,
emotions often start with an appraisal, and basic emotions
systems can be thought of as having an appraisal mechanism at
their front end.
But further thought suggests that the basic emotions approach
might not be quite right for either the Scarantino (2012) or the
Mulligan and Scherer (2012) model. Lets look at why in some
detail by making things very concrete. This will be done by
considering fear and the brain in some detail.

Fear (Defense) and the Brain

Relevance to the Target Articles

Dixons (2012) interesting article concludes that the term
emotion does not refer to something that constitutes a natural
kind. Challenges to the natural kind status of emotion have come
up many times, and take various shapes (e.g., Barrett, 2006;
Izard, 2007; Scarantino, 2012). The version Dixon prefers is that
emotion should be divided into categories, such as basic and
higher cognitive emotions (Griffiths, 1997, 2004), that might be
natural kinds.
Scarantino (2012) also is skeptical of the idea that emotion
is a natural kind, but goes further than Dixon in arguing that even
the category of basic emotions is not a natural kind since the
specific emotions that constitute basic emotions are themselves
not natural kinds. But he does not go as far as Barrett (2006) in
rejecting the entire notion of basic emotions. Instead, he feels
that some emotions are basic and do form a natural kind set, but
that a new conceptualization of what basic means is needed.
Mulligan and Scherer (2012) argue that emotions are, at a
minimum, psychological kinds. They give several criteria that
identify components that occur in and define what emotions
are psychologically. A key component is appraisal. The way
situations are appraised allows the coordinated activity of the
various components of emotion to operate in a way that produces
specific emotions. Appraisal and coordinated activity are key
concepts in their proposal.
How does all this relate to the brain models discussed before?
Any approach that accepts the validity of the basic emotions
concept, namely the idea that basic emotions form a limited and
natural set of emotions, is most compatible with a basic emotions
approach to brain mechanisms, where each basic emotion has its
own neural representation. The one-size-fits-all approach of the
limbic system is not going to work in a basic emotions theory since
it assumes one system for all emotions. The emotions-one-at-atime approach also wont work very well as an accompaniment to
a psychological approach that is centered on basic emotions since
it does not compare and contrast across emotion systems to define
the set of emotions that are basic. So both the Dixon (2012) and
Scarantino (2012) pieces would seem to be most compatible with
a basic emotions approach to the brain.
On the other hand, something like the limbic system theory
could be compatible with the Mulligan and Scherer (2012) idea

As noted above, much of what has been learned about the fear
or defense system comes from studies of Pavlovian defense
(fear) conditioning. Once a conditioned threat is created as a
result of a neutral stimulus being associated with danger, the
conditioned stimulus will elicit defense responses via a wellestablished set of pathways in the brain that have been
implicated in fear by the consistency and convergence of
conclusions across a variety of methodologies (electrolytic
and neurotoxic lesions; electrophysiological recordings;
anatomical tracing; pharmacological, molecular, and genetic
manipulations; functional imaging) (see Johansen et al., 2011;
LeDoux, 2000; Maren, 2005; Phelps, 2006; Rodrigues, Schafe,
& LeDoux, 2004).
We often hear that the amygdala is involved in fear or other
emotions. But this is way too crude a conclusion. Very restricted
components of the amygdala (subpopulations of neurons in
subareas of amygdala areas) are involved. Only by applying the
techniques of modern neuroscience can such conclusions be
drawn.
Information about the learned (conditioned) threat is transmitted
from sensory processing systems to the lateral amygdala, where
the stimulus is assessed (appraised). Through the conditioning
process, the stimulus has acquired the ability to activate lateral
amygdala neurons in such a way as to initiate a cascade of
subsequent processing in the amygdala and beyond. Specifically,
by way of connections (direct and indirect) from the lateral nucleus
to the central nucleus, and from there to specific downstream areas
that control different response modalities, behavioral, autonomic,
and endocrine responses are triggered in the effort to cope with the
danger. Particularly impressive has been the degree to which
modern neuroscience methods have been able to implicate specific
neurons within subareas of amygdala nuclei (i.e., subareas within
the lateral and central nuclei) and the molecular mechanisms that
mediate communication within and between these neurons (e.g.,
fear learning depends on synaptic plasticity in neurons in the
superior part of the dorsal subnucleus of the lateral nucleus, and
the expression of fear behavior involves specific neurons within
the medial division of the central nucleus).
In addition to connections to output areas, the central nucleus
has connections to brainstem arousal systems. When these
are activated, neuromodulators (norepinephrine, dopamine,

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378 Emotion Review Vol. 4 No. 4

acetylcholine, serotonin, etc.) are released widely in the brain,

including in cognitive processing regions in the cortex. The
areas affected are put on alert (are aroused in a nonspecific
way). That is, their cells are primed for information processing.
Various amygdala areas also project directly to cortical areas
and can influence processing this way as well. A global state
of readiness results in which attention, perception, memory
retrieval, and memory formation are all facilitated.
The overall effects are thus twofold. Defensive behavior is
elicited and the brain is globally activated. Because this global
activity is occurring simultaneously in widespread areas
involved in diverse functions, you could say that activity is
coordinated in the brain, as Scherer has argued (Scherer, 1984),
and could even say that brain activity is monopolized by
emotional arousal, as I have argued (LeDoux, 2002).
The term motive state has sometimes been used to refer to
global brain states associated with emotion and motivation
(Bindra, 1969; Hebb, 1949; Morgan, 1943). Emotive state might
be a better term. Such states likely underlie (or at least make
significant contributions to) what we call feelings or subjective
emotional experiences in humans. But a motive or emotive state
is a physical state of the brain that, unlike feelings, can
potentially be measured in humans and animals alike.
One way of interpreting the foregoing is that fear is a basic
emotion mediated by a specific circuit built into the brain and
thus qualifies as a natural kind. But I wouldnt put it that way. I
would instead say that there are phenomena that are talked
about under the topic of fear that are products of specific circuits
in the brain, but that these dont qualify as a single unified state
of fear in the usual sense of the term. Specifically, there are a
variety of phenomena that fall under the rubric fear that have
different neural requirements. For example, defense responses
elicited by conspecific or predator odors, which are innate fear
stimuli, require different circuits (Choi et al., 2005; Markham,
Blanchard, Canteras, Cuyno, & Blanchard, 2004; Motta et al.,
2009) than those just described for learned cues. States where
harm is possible but unpredictable (more like anxiety than fear)
involve still different circuits (Davis, Walker, & Lee, 1997).
Completely different circuits are likely to be required to fear
falling in love or to fear fear itself (the latter two states are more
like the cognitive emotions that Dixon [2012] discussed).
Ekmans notion of emotion families (Ekman, 1999) might work
as a psychological grouping of these diverse phenomena, but it
is unlikely that the various phenomena have much in the way of
a unified biological basis.

Conclusion
Because of the heterogeneity of such a seemingly simple and
basic emotion as fear at the neural level, I doubt that a basic
emotions approach to the brain will work. In fact, I believe the
only approach that works is a one-emotion-at-a-time approach,
with the term emotion not referring to common language notions
like fear, anger, or joy, but to states that contribute to survival
(defense, reproduction, energy homeostasis, etc.) (LeDoux,
2012). The states should be studied in terms of specific kinds of

experimental tasks designed for the purpose of identifying

specific circuits and microcircuits, much in the way that learned
and unlearned fear has been studied. This may be unsatisfying
from the point of view of an immediate, all-encompassing
theory of emotion, but in the long run might provide a basis for
a viable natural kinds approach to emotional phenomena (if not
emotion itself) centered on brain circuits.

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