The Emotional Brain, Fear, and the Amygdala
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The Emotional Brain, Fear, and the Amygdala
SUMMARY
1. Considerable progress has beenmadeover the past 20 years in relating specific circuits
of the brain to emotional functions. Much of this work has involved studies of Pavlovian
or classical fear conditioning, a behavioral procedure that is used to couple meaningless
environmental stimuli to emotional (defense) response networks.
2. The major conclusion from studies of fear conditioning is that the amygdala plays
critical role in linking external stimuli to defense responses.
3. Before describing research on the role of the amygdala in fear conditioning, though,
it will be helpful to briefly examine the historical events that preceded modern research on
conditioned fear.
KEYWORDS: emotion; amygdala; limbio system; fear.
THE EMOTIONAL BRAIN IN PERSPECTIVE
In the early part of the twentieth century, researchers identified the hypothalamus
as a key structure in the control of the autonomic nervous system (Karplus and
Kreidl, 1927). On the basis of these early observations, and their own work (Cannon
and Britton, 1925), Cannon and Bard proposed a hypothalamic theory of emotion
that consisted of three major points: (1) the hypothalamus evaluates the emotional
relevance of environmental events; (2) the expression of emotional responses is
mediated by the discharge of impulses from the hypothalamus to the brainstem;
(3) projections from the hypothalamus to the cortex mediate the conscious experience
of emotion (Bard, 1928; Cannon, 1929). In 1937 Papez added additional anatomical
circuits in the forebrain to the theory, but retained the central role of ascending
and descending connections of the hypothalamus. The Papez theory, in turn, was
extended by MacLean (1949, 1952), who called the forebrain emotional circuits the
visceral brain, and later, the limbic system.
Although the term limbic system is still used to refer to the emotional circuits of
the brain, the limbic system theory has come under attack on several grounds (see
Brodal, 1980; Kotter and Meyer, 1992; LeDoux, 1987, 1991, 1996; Swanson, 1983).
1 Center for Neural Science, New York University, New York.
2To whom correspondence should be addressed at Center for Neural Science, New York University, New
York; e-mail: ledoux@cns.nyv.edu
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0272-4340/03/1000-0727/0 CÐ'o 2003 Plenum Publishing Corporation
728 LeDoux
First, there are no widely accepted criteria for deciding what is and what is not a
limbic area. Second, however defined, the limbic system theory does not explain
how the brain makes emotions. It points to a broad area of the forebrain located
roughly between the neocortex and hypothalamus, but does not account for how
specific aspects of any given emotion might be mediated.
The amygdala was part of the MacLean’s limbic system theory. However, it did
not stand out as an especially important limbic area until 1956 when Weiskrantz
showed that the emotional components of the so-called Kluver and Bucy syndrome
(Kluver and Bucy, 1937), a constellation of behavioral consequences of temporal lobe
damage, were due to the involvement of the of the amygdala. Weiskrantz proposed
that amygdala lesions dissociate the affective or reinforcing properties of stimuli
from their sensory representations.
THE AMYGDALA AND FEAR CONDITIONING
In the years following Weiskrantz’s publication, a number of studies pursued
the role of the amygdala in fear by using a variety of different approaches. However,
no consistent conclusions emerged, in large part because complex behavioral
tasks that varied considerably from study to study were used. In short, there was
little appreciation that different emotional tasks would be mediated by the brain in
unique ways. Then, in the late 1970s and early 80s, researchers began using a simple
behavioral task, Pavlovian fear conditioning, to study fear networks. This made all
the difference.
In Pavlovian fear conditioning, an emotionally neutral conditioned stimulus
(CS), usually a tone, is presented in conjunction with an averisve unconditioned
stimulus (US), often footshock. After one or several pairings, the CS acquires the
capacity to elicit responses that typically occur in the presence of danger, such as
defensive behavior (freezing or escape responses), autonomic nervous system responses
(changes in blood pressure and heart rate), neuroendocrine responses (release
of hormones from the pituitary and adrenal glands), etc. The responses are not
learned and are not voluntary. They are innate, species-typical responses to threats
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