Amygdala, Primate

For more than one century there has been evidence that the amygdala is involved in emotional behavior. Experimental lesion studies in monkeys demonstrated that large temporal lobe lesions that included the amygdala resulted in dramatic postoperative changes in behavior, including flattened affect, visual agnosia, hyperorality, and hypersexuality (Brown and Schaefer 1888; Klüver and Bucy 1938). Similar behaviors have also been observed in humans with large temporal lobe lesions that include the amygdala (Terzian and Dalle Ore 1955). The amygdala was more formally linked to emotional behavior in 1949, when Paul MacLean expanded Papez's notion of the LIMBIC SYSTEM to include this region, based on neuroanatomical criteria. Over the past several decades, converging results of neuroanatomical, behavioral, and physiological studies in macaque monkeys along with neuropsychological and neuroimaging studies in humans have firmly established a role for the amygdala in emotional processing. However, a number of important questions remain regarding the nature and specificity of this role. In addition, the amygdala has also been linked to social behavior but these data will not be reviewed here. In this article, a brief neuroanatomical review will be followed by a survey of two areas of particularly active research involving the primate amygdala: expression of emotional behavior and the recognition of facial emotion.

The unique neuroanatomical profile of the amygdala illustrates why this structure has been referred to as the "sensory gateway to the emotions" (Aggleton and Mishkin 1986). The amygdala comprises at least thirteen distinct nuclei, each with a rich pattern of intrinsic connections. As to extrinsic connections, the amygdala is directly interconnected with unimodal and polymodal sensory cortical areas as well as with subcortical structures such as the basal forebrain, THALAMUS, hypothalamus, striatum, and brainstem areas. Thus, the amygdala is centrally positioned to receive convergent cortical and thalamic sensory information and subsequently to direct the appropriate survival-oriented response via its brainstem and hypothalamic projections. Moreover, the significant neuroanatomical connections between the amygdala and nearby medial temporal lobe regions involved in MEMORY may provide the substrate for the enhancing effect of emotional arousal on memory, as demonstrated by a significant body of animal and human studies (McGaugh et al. 1995; Cahill et al. 1995).

Experimental lesions that target the amygdala have produced many of the behaviors that were originally described after the large lesions of Klüver and Bucy and Brown and Schaefer (Weiskrantz 1956; Aggleton, Burton, and Passingham 1980; Zola-Morgan et al. 1991). However, due to methodological difficulties, these lesions typically have included inadvertent cortical and/or fiber damage; thus, interpretations of amygdala function based on these classic studies alone must be made with caution. Highly circumscribed amygdala lesions can now be produced using the neurotoxic lesion technique, and results from these studies indicate a role for the amygdala in temperament and oral exploration (Amaral et al. 1997), food preferences (Murray, Gaffan, and Flint 1996), and in the devaluation of a food reward after selective satiation (Malkova, Gaffan, and Murray 1997).

Interestingly, the behavioral changes observed after neurotoxic amygdala lesions are much less profound than those that were reported using more traditional (i.e., less discrete) lesion techniques. The perirhinal cortex, known to be important for memory (Zola-Morgan et al. 1989), lies adjacent to the amygdala, and these two regions are strongly neuroanatomically interconnected (Stefanacci, Suzuki, and Amaral 1996). It has been suggested that the amygdala and the perirhinal cortex may have some shared roles in emotional behavior (Iwai et al. 1990; Stefanacci, Suzuki, and Amaral 1996). Thus, it is possible that dramatic emotional changes may occur only after lesions that include both of these regions.

Recent studies in humans have explored the role of the amygdala in the recognition of facial emotion and of the recognition of fear in particular (see EMOTION AND THE HUMAN BRAIN). Taken together, the evidence is not entirely supportive. On the positive side, one study reported that a patient with relatively discrete, bilateral amygdala damage as determined by MAGNETIC RESONANCE IMAGING (MRI) was impaired at recognizing fear in facial expressions (Adolphs et al. 1994). A second patient who has partial bilateral amygdala damage, determined by MRI, was similarly impaired (Calder et al. 1996) and was also impaired in recognizing fear and anger in the auditory domain (Scott et al. 1997). However, this patient also has more general facial and auditory processing impairments (Young et al. 1996; Scott et al. 1997).

Functional neuroimaging data provide additional support for the notion that the amygdala is preferentially involved in the recognition of fearful versus happy faces (Morris et al. 1996). However, the results from other studies are not consistent with this notion. First, recognition of facial emotion, including fear, may occur even in the absence of the amygdala (Hamann et al. 1996). Second, single neurons in the human amygdala respond to particular facial expressions but do not respond exclusively to fearful expressions (Fried, MacDonald, and Wilson 1997). In monkeys, there is a population of amygdala neurons that respond selectively to faces (Leonard et al. 1985), but there is little or no evidence to support the idea that these neurons respond selectively to fearful expressions. Finally, functional magnetic resonance imaging (fMRI) has revealed increased activation in the amygdala in response to both happy and fearful faces (Breiter et al. 1996).

To conclude, studies in monkeys and humans over the past several decades have reinforced the long-held view, supported by findings in other species (see EMOTION AND THE ANIMAL BRAIN), that the amgydala has an important role in emotional function. New experimental approaches, such as functional neuroimaging and the use of highly selective lesion techniques, hold promise for an exciting new era of progress that builds on this work.

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AMYGDALA

-- Lisa Stefanacci

References

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Zola-Morgan, S., L. R. Squire, D. G. Amaral, and W. A. Suzuki. (1989). Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment. J. Neurosci 9:4355-4370.

Amygdala, Primate

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