Emotion Systems and the Brain
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Emotion Systems and the Brain
J LeDoux, New York University, New York, NY, USA
ã 2009 Elsevier Ltd. All rights reserved.
aimed at revealing the brain mechanisms is summarized through which emotional responses are controlled by external stimuli.
Unconscious Emotional Processing
Introduction
In 1884, William James asked, “What is an emotion?”
Although his answer was not universally accepted, the
way James framed the problem continues to influence
how we think about emotions today. Particularly
important was James’ distinction between the bodily
expression of emotions and conscious emotional
experiences or feelings.
James’ goal was to explain feelings. But to do so,
he felt he had to first dispel the common sense notion
that feelings cause us to behave in certain ways. He
argued that this was flat out wrong – in fact, backwards.
In his view, the expression of an emotion in behavior
and other physiological responses of the body actually
determine what we feel. James’ paper gave rise to two
questions that have occupied emotion researchers and
theorists ever since. One is, “how do emotional stimuli
elicit emotional responses?” The other is, “what are
feelings?” The first is a relatively straightforward empirical question. The second is considerably more complicated. In this overview of emotion concepts, this
article begins by summarizing progress that has been
made on these two questions. This article also discusses
how the two questions sometimes get confused.
How Do Emotional Stimuli Elicit Emotional
Responses?
James put his finger on a very important point when
he rejected the idea that feelings cause emotional
responses. Because different emotions (say, fear vs.
joy) are elicited by different kinds of stimuli, the
brain must have already determined the emotional
nature of the situation before the feeling or the
response occurs. James did not dwell on this, since
he wanted to know what causes feelings. But implicit
in his formulation was the notion that emotional
responses are elicited on the basis of unconscious
processing of emotional stimuli, since the conscious
aspect of emotion, the feeling, does not emerge until
the responses are expressed. Regardless of whether
you accept James’ theory, unless you accept the common sense view, that feelings cause responses, unconscious emotional processing must be the basis of
the responses. The following sections, outline how
emotional stimuli, via unconscious processes, lead to
the expression of emotional responses. Then, research
In the first half of the twentieth century, behaviorists
eliminated ‘consciousness’ from psychology and only
allowed the description of psychological processes in
terms of observable behavior. With the rise of cognitive
science, the possibility arose for viewing psychological
functions in terms of internal representations, without
equating those internal processes with consciousness.
That is, psychological functions involve information
processing. Such processing could, but does not have
to, lead to conscious experiences. Information processing, in other words, is by definition unconscious. This
notion was originally about cognitive processes such as
perception and memory, but it was subsequently
extended to emotional processing.
The processing of emotional stimuli is typically
referred in psychology to as ‘evaluative processing,’
or appraisal. Appraisal is said to underlie both the
emotional responses and the conscious feelings that
occur in the presence of emotional stimuli. Nevertheless, appraisal theorists have traditionally focused on
the role of appraisals in feelings, and have viewed
appraisals in terms of higher cognitive processes.
However, as we will see, basic evaluative or appraisal
mechanisms that operate unconsciously are also
involved in the elicitation of emotional responses by
external stimuli.
Everyone has, in some situation, found his or
her heart pounding before recognizing the nature
of the eliciting event. Considerable scientific evidence
also supports the idea that unconsciously processed
stimuli can control emotional responses. This does
not mean that conscious appraisal never occurs.
It simply means that conscious appraisal is not necessary for the elicitation of emotional responses. The
idea that emotional responses are based on unconscious appraisal processes is actually of tremendous
value from the point of view of brain research. It
allows us to do research on emotional behavior without having to first solve the mind–body problem, and
allows us to treat the control of emotional responses
in animals and humans similarly.
There are two basic ways in which emotional
stimuli can elicit emotional responses by activating
appraisal mechanisms. Some appraisals are hardwired by evolution and others are learned through
individual experience. All organisms, including humans,
have innate appraisal capacities that help ensure their
survival. Stimuli that signal sexual partners, palatable
904 Emotion Systems and the Brain
and poisonous foods, painful stimulation, predators,
or aggressive members of one’s own species are common examples. Such stimuli activate innate appraisal
mechanisms and lead directly to the expression of
species-typical responses and accompanying autonomic responses. For example, a rat that encounters
a cat for the first time will express signs of fear, even
if it was reared in a laboratory and never previously
exposed to a cat. When organisms encounter stimuli
that innately activate appraisal mechanisms they
often form associations (through Pavlovian conditioning) with other stimuli present, since these may
be predictive of harm or benefit in the future. These
conditioned stimuli acquire the capacity to elicit
species-typical emotional responses.
Species-typical behavioral and autonomic responses
are often just the first stage of emotional responding to an innate or conditioned emotional stimulus.
In addition to these reactions, organisms also often
perform instrumental actions. Avoidance behavior
is a canonical example of a learned aversive instrumental action. Thus, when you encounter an innate
or conditioned danger signal, your first reaction may
be to freeze. But you may also try to escape from
or avoid the danger. Sometimes avoidance of danger becomes pathological, as when a patient with
panic disorder stays inside her home in order to reduce
the chances of having an attack. Positive instrumental responses are also important. We seek stimuli
and situations that lead to desirable outcomes. But
these too can have pathological consequences. Eating
disorders and drug addiction are common examples.
Instrumental responses are often learned through
trial-and-error processes in which the probability
of the response changes depending on the rewarding
or punishing consequences of the behavior. Once
learned, these are performed as habits. However,
instrumental responses can also be based on spontaneous decisions; cognitive estimation of outcomes
eliminates the need for trial-and-error leaning.
In summary, the brain unconsciously appraises
the value of external stimuli. Some stimuli are significant because of innate wiring, while the significance
of others is learned through experience. Stimuli
that are appraised as significant then lead to the
expression of responses. Both innate and learned
stimuli can lead to the expression of hard-wired
species-typical emotional responses. These reactions
are then often followed by instrumental responses
that reflect past learning or spontaneous decisions.
Brain Mechanisms of Emotional Processing
William James not only speculated about the nature
of emotion, he also proposed the first modern brain
theory of emotion. By the late nineteenth century
researchers had discovered sensory and motor regions
in the cortex. James therefore asked whether an emotion ‘center’ was yet to be discovered or whether it
might be possible to explain emotions as functions of
cortical sensory and motor areas. He preferred the
latter idea, arguing that emotional stimuli elicit emotional responses by way of sensory cortex activation
of motor cortex. This idea was then challenged by
Walter Cannon on the basis of studies showing that
emotional reactions were preserved in decorticate
animals, but were disrupted after damage to the
hypothalamus. On the basis of these and other observations, Papez, in 1937, proposed a circuit theory of
emotion involving the hypothalamus, anterior thalamus, cingulate gyrus, and hippocampus. Later,
MacLean then named the structures of the Papez
circuit, together with several additional regions
(amygdala, septal nuclei, orbitofrontal cortex, portions of the basal ganglia), the limbic system, which
he viewed as a general-purpose system involved in
behaviors that ensure survival of the individual and
the species.
MacLean’s writings were very persuasive and
for many years the problem of relating emotion to
brain mechanisms seemed solved at the level of anatomical systems. However, the limbic system concept
is now believed to suffer from imprecision at both
the structural and the functional levels. For example,
it has proved impossible to provide unequivocal criteria for defining which structures and pathways
should be included in the limbic system. A standard
criterion is connectivity with the hypothalamus. However, because studies have shown that the hypothalamus is connected with structures at all levels of
the central nervous system, from the neocortex to the
spinal cord, the limbic system would occupy much of
the brain. Further, classic limbic areas, such as the
hippocampus and mammillary bodies, have proved
to be far more important for cognitive processes,
such as declarative memory, than for emotional
processes.
The post-Jamesian theories of the emotional brain
were fairly consistent in their view of how sensory
stimuli lead to the expression of emotional responses.
Sensory information transmitted from the thalamus
and/or cortex to specialized subcortical emotion circuits regulates the expression of emotional responses.
In these theories, the subcortical circuits were centered
on the hypothalamus. Electrical stimulation studies
provided strong support for the role of the hypothalamus in the control of emotional responses, including
autonomic responses.
Today, the emphasis has shifted from the hypothalamus to the amygdala, especially in the control
Emotion Systems and the Brain
of the bodily responses that occur during fear reactions in both animals and humans. The animal studies
indicate that one region of the amygdala, the lateral
nucleus, receives sensory information from the thalamus and cortex. It then connects with the central
amygdala, which in turn connects with lower areas,
including the hypothalamus, that then connect
with specific motor neuron groups that control emotional responses. Circuits within the amygdala in
essence mediate the appraisal of danger, including
learning about stimuli associated with danger. The
amygdala has also been implicated in appraising
positive emotional stimuli, but the circuit details
are less well understood.
The scenario just described mainly applies to aversive emotional responses that are elicited automatically in response to a stimulus. But, as noted earlier,
in addition to reacting in an automatic fashion to
emotional events, organisms also perform instrumental responses. The amygdala is also involved
in instrumental responses, but in a different way
than for automatically elicited responses. Specifically, the central amygdala and its connectivity
with lower brain regions is not involved. Instead,
connections from the lateral nucleus to the basal
amygdala, and from there to the striatum, seem to
be important.
A prominent idea in recent years has been that
the prefrontal cortex, especially the ventromedial
prefrontal cortex, interacts with the amygdala in
the regulation of emotional responses. The amygdala
is often thought of as an emotional accelerator and
the prefrontal cortex as the brakes. Prefrontal cortex
is also likely to play an important role in the decisionmaking processes through which instrumental behavior is regulated in emotional situations.
In summary, much has been learned about the
neural circuits through which sensory stimuli come
to elicit emotional responses. Progress has been
made for both negative and positive emotions, and
for both automatic and instrumental responses.
What Are Feelings?
As noted previously, what William James really cared
about was the nature of feelings. And throughout the
following century, up to this day, there has been much
debate about just what feelings are, both in psychology and brain science.
The Psychology of Feelings
After several decades of acceptance, James’ theory
of feelings was dethroned by Walter Cannon. He
rejected the idea that feelings are due to feedback
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from responses, since, he said, the bodily responses
would be too slow and too vague to define the difference between fear and joy and love and grief.
The debate stalled for decades, but took a new turn
in the 1960s when Stanley Schachter and Jerome
Singer proposed that both James and Cannon were
right. Cannon was right that body arousal is not
specific enough. James was right that body arousal
was important. The solution, they said, was that
through cognitive processes we interpret nonspecific
body arousal in light of the context which exists at the
moment. Later theories eliminated the need for bodily
responses at all, emphasizing the importance of cognitive processing.
By the 1980s, emotion had become a full-fledged
cognitive process. Some, such as Robert Zajonc, felt
this went too far. On the basis of the results of clever
experiments he performed, Zajonc argued that feelings are the products of unconscious affect. Because
he objected to the cognitive take over of emotion,
he avoided the use of the term unconscious processing. Nevertheless, his work made the idea that conscious feelings might be based on unconscious
appraisal palatable.
Feelings and the Brain
The various aforementioned theories of the emotional
brain each proposed that feelings are products of information processing in the cerebral cortex. For Cannon,
feelings occurred in this way: sensory information split
at the thalamus, with some going to the hypothalamus
and some to the cortex. The hypothalamus then communicated with the cortex. When hypothalamic information interacted with sensory information in the
cerebral cortex, a feeling was the result. Papez had a
similar theory, but with more anatomical specificity,
proposing that feelings occurred when the cingulate
cortex integrated external sensory information with
information processed by the hypothalamus. For
MacLean, feelings resulted in the limbic system when
the hippocampal cortex integrated information from
the internal and external environments.
After several decades of dormancy, research and
theory on the brain mechanisms of emotion began
to pick up in 1980s. For the most part, this work
was focused on emotional learning and the control
of emotional behavior. However, attention was also
returning to questions about the nature of feelings.
William James, you’ll recall, proposed that feelings
result when the cortex perceives body sensations
produced during an emotional reaction. Thus, fear
feels different from love because these two emotions
have different effects on the body. Although James
emphasized the entire bodily response, critics such
906 Emotion Systems and the Brain
as Cannon focused on the autonomic nervous system
response. While autonomic responses are indeed slow
and nonspecific, feedback from the muscles through
proprioception can be fast and specific. A contemporary theory that emphasizes such responses is the
facial feedback hypothesis. This theory proposes that
the specific facial responses associated with certain
emotions provide feedback to the brain that determines what we feel. Another feedback theory was
proposed in 1994 by Antonio Damasio. Building
on James, Damasio argued that we use ‘gut feelings’
to figure out what we are feeling, and that this
information plays an important role in the way we
make decisions. For example, when trying to decide
between two courses of action, we play these out
in our minds and the body sensations that result in
one versus the other, according to Damasio, help us
decide which to choose (which one ‘feels’ better).
According to Damasio, the orbitofrontal cortex and
the body-sensing regions of the cortex (somatosensory and insular regions) are involved in feeling states.
From authors viewpoint, feedback from the body
such as that described by James and Damasio adds
intensity and duration to emotional experiences, but
the quality of the experience is a product of working
memory. Because working memory is believed to be
the cognitive operation that makes consciousness
possible, it may be the basis of conscious feelings as
well as cognitive states of consciousness. The basic
idea is that we have one mechanism of consciousness,
and qualitatively different states of consciousness are
defined by the kind of information that we are conscious of at the moment. Through working memory
we are able to integrate the way something looks and
sounds with past memories of this thing, and with
the way this thing is making us feel at the moment. If
you encounter a rattlesnake on a path, for example,
the following kinds of information will likely come
to be present in working memory: a visual representation of the snake, an auditory representation of
the rattling sound, information retrieved from longterm memory (things known about snakes as well
as experiences with them), and information about
the state of your brain (the fact that a certain emotion
system is activated and that you are aroused). These
will combine to produce an integrated representation
in working memory of the entire experience. The
cognitive appraisal of this experience in working
memory is the initial feeling. At the same time, bodily
responses, which are slower to occur, are expressed.
These then feed back to the brain and add to the
feeling that is evolving. The difference between an
emotional conscious experience and a nonemotional
one is simply that working memory is working with
additional information in the case of the emotional
experience – namely, information about the emotional
aspects of the experience. The difference between different kinds of emotional experiences (fear vs. joy) is
due to the particular emotion system that is active at
the moment and monopolizing consciousness.
Considerable evidence implicates the dorsolateral
prefrontal cortex (PFC) in working memory. While
the brain networks of working memory were once
narrowly viewed as mainly involving the dorsolateral
PFC, this is no longer the case. The various medial
areas of PFC, including the orbital cortex and anterior
cingulate, as well as insular cortex, are now viewed
as being involved, especially in emotional situations.
This broader view of working memory overlaps with
Damasio’s somatic hypothesis but without placing
too much burden on peripheral feedback.
Can Responses Tell Us about Feelings?
A final issue to consider is the relation of responses
and feelings. This issue has two parts. One has
already been discussed: do responses cause feelings?
James and Damasio emphasize this view. Others take
issue with it. But the part that we want to consider
here is this: can responses tell us what other organisms are feeling?
Some years ago, Nagel pointed out that each
species is likely to have its own kind of subjective
experience of world. Because working memory plays
a key role in human conscious awareness of the
world, the brain mechanisms of working memory
may give us clues about the kinds of experiences
different organisms can have. Interestingly, the brain
regions involved in working memory are more highly
developed in humans than in other primates and more
highly developed in other primates than in other
mammals. Adding in the fact that language is likely
to change the way experiences are interpreted (and
appraised), and that only humans have natural language, we are led to the conclusion that whatever
kinds of experiences other organisms have, they
are likely to be distinct from those typical of humans.
The bottom line is that two organisms may have
identical behavioral and autonomic responses but
have completely different conscious experiences. You
can trust to some extent that when another human
is acting fearful or joyful they are likely to be feeling
what you refer to as fear or joy. The reason we can
trust this conclusion is because we have the same
basic brain plan as do other members of our species.
We can therefore take what we know from our own
experiences and apply it to others. We do this all
the time in social interactions. People also often do
this for pets and other animals. The reason this
‘anthropomorphic’ reasoning is inappropriate was
Emotion Systems and the Brain
explained earlier: because the brain mechanisms of
consciousness are likely to be different in different
organisms, mainly because of the development of the
prefrontal cortex in primates and language in humans,
conscious experiences are likely to be different.
Conclusion
This brief survey, much of it including historical
material, provides an overview of some of the major
concepts of emotion that are relevant to the pursuit of
brain mechanisms of emotion. Many of these concepts have been explored in depth in the large body
of literature on emotion theory.
See also: Aggression: Hormonal Basis; Aggression:
Neurochemical and Molecular Mechanisms; Amygdala:
Contributions to Fear; Aversive Emotions: Molecular
Basis of Unconditioned Fear; Aversive Emotions: Genetic
Mechanisms of Serotonin; Emotion and Vigilance;
Emotion in Speech; Emotion: Neuroimaging; Emotion:
Computational Modeling; Emotional Disorders:
Treatment; Emotional Hormones and Memory
Modulation; Emotional Influences on Memory and
Attention; Emotional Control of the Autonomic Nervous
System; Genetics of Human Anxiety and Its Disorders;
Social Emotion: Neuroimaging.
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