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Purves D, Augustine GJ, Fitzpatrick D, et al., editors. Neuroscience. 2nd edition. Sunderland (MA): Sinauer Associates; 2001.

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Neuroscience. 2nd edition.

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The Importance of the Amygdala

Experiments first performed in the late 1950s by John Downer at University College London vividly demonstrated the importance of the amygdala in aggressive behavior. Downer removed one amygdala in rhesus monkeys, at the same time transecting the optic chiasm and the commissures that link the two hemispheres (see Chapter 27). In so doing, he produced an animal with a single amygdala that had access only to visual inputs from the eye on the same side of the head. Downer found that the animals' behavior depended on which eye was used to view the world. When the eye on the side of the intact amygdala was covered, the monkeys behaved in some respects like the monkeys described by Klüver and Bucy; for example, they were relatively placid in the presence of humans. If, however, they were allowed to see only with the eye on the side of the intact amygdala, they reverted to their normal fearful and often aggressive behavior. Thus, in the absence of the amygdala, a monkey does not interpret the significance of the visual stimulus presented by an approaching human in the same way as a normal animal. Importantly, only visual stimuli presented to the eye on the side of the ablation produced this abnormal state; thus if the animal was touched on either side, a full aggressive reaction occurred, implying that somatic sensory information about both sides of the body had access to the remaining amygdala. Taken together, these results show that the amygdala mediates processes that invest sensory experience with emotional significance.

To better understand the role of the amygdala in evaluating stimuli, and to define more precisely the specific circuits and mechanisms involved, several other animal models of emotional behavior have been developed. One of the most useful is based on conditioned fear responses in rats. Conditioned fear develops when an initially neutral stimulus is repeatedly paired with an inherently aversive one. Over time, the animal begins to respond to the neutral stimulus with behaviors similar to those elicited by the threatening stimulus (i.e., it learns to attach a new meaning to it). Studies of the parts of the brain involved in the development of conditioned fear in rats have begun to shed some light on this process. Joseph LeDoux and his colleagues at New York University trained rats to associate a tone with a foot shock delivered shortly after onset of the sound. To assess the animals' responses, they measured blood pressure and the length of time the animals crouched without moving (a behavior called “freezing”). Before training, the rats did not react to the tone, nor did their blood pressure change when the tone was presented. After training, however, the onset of the tone caused a marked increase in blood pressure and prolonged periods of behavioral freezing. Using this paradigm, LeDoux worked out the neural circuitry that established the association between the tone and fear (Figure 29.5). First, he demonstrated that the medial geniculate nucleus is necessary for the development of the conditioned fear response. This result is not surprising, since all auditory information that reaches the forebrain travels through the medial geniculate nucleus of the dorsal thalamus (see Chapter 13). He went on to show, however, that the responses were still elicited if the connections between the medial geniculate and auditory cortex were severed, leaving only a projection between the medial geniculate and the amygdala. Furthermore, if the part of the medial geniculate that projects to the amygdala was also destroyed, the fear responses were abolished. Subsequent work in LeDoux's laboratory established that projections from the amygdala to the midbrain reticular formation are critical in the expression of freezing behavior, and that projections from the amygdala to the hypothalamus control the rise in blood pressure.

Figure 29.5. Pathways in the rat brain that mediate the association of auditory and aversive stimuli.

Figure 29.5

Pathways in the rat brain that mediate the association of auditory and aversive stimuli. Information processed by the auditory centers in the brainstem is relayed to the auditory cortex via the medial geniculate nucleus (1). The amygdala receives auditory (more...)

Since the amygdala is a site where neural activity produced by both tones and shocks can be processed, it is reasonable to suppose that the amygdala is also the site where learning about fearful stimuli occurs. These results, among others, have led to the broader hypothesis that the amygdala participates in establishing associations between neutral sensory stimuli, such as a mild auditory tone or the sight of inanimate object in the environment, and other stimuli that have some primary reinforcement value (Figure 29.6). The neutral sensory stimuli can be stimuli in the external environment, stimuli communicated centrally via the special sensory afferent systems, or internal stimuli derived from activation of visceral sensory receptors. The stimuli with primary reinforcement value include sensory stimuli that are inherently rewarding, such as the sight, smell, and taste of food, or stimuli with negative values such as an aversive taste, loud sounds, or painful mechanical stimulation. The associative learning process itself is probably a Hebbian-like mechanism (see Chapters 24 and 25) that strengthens the connections relaying the information about the neutral stimulus, provided that they activate the postsynaptic neurons in the amygdala at the same time as inputs pertaining to the primary reinforcer. The discovery that long-term potentiation (LTP) can be evoked in the amygdala provides further support for this hypothesis. Indeed, the acquisition of conditioned fear in rats is blocked by infusion into the amygdala of NMDA antagonists, which prevents the induction of LTP. Finally, the behavior of patients with selective damage to the anterior-medial temporal lobe indicates that the amygdala plays a similar role in the human experience of fear (Box D).

Figure 29.6. Model of associative learning in the amygdala relevant to emotional function.

Figure 29.6

Model of associative learning in the amygdala relevant to emotional function. Neutral sensory inputs are relayed to principal neurons in the amygdala by projections from “higher order” sensory processing areas that represent objects (e.g., (more...)

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Box D

Fear and the Human Amygdala: A Case Study.

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Copyright © 2001, Sinauer Associates, Inc.
Bookshelf ID: NBK10891

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