Cellular and Molecular Neurobiology

The Emotional Brain, Fear, and the Amygdala

By Joseph LeDoux



SUMMARY

Considerable progress has been made over 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.

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).

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.

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