The amygdala, social behavior, and danger detection

The amygdala is a distinctive portion of the anterior temporal lobe that has been implicated in a variety of functions including expression of fear, modulation of memory, and mediation of social communication. While work on the rodent amygdala often deals with emotion, much of the research in nonhuman primates and in man deals with its role in the perception of social signals, such as facial expressions, and the maintenance of social position, such as in primate dominance hierarchies. We have established a program of research that has as its major goal the definition of neural systems that underlie species-typical social communication. A first phase of the program was launched on the premise that the amygdala is essential for species-typical social behavior. We sought to examine in more detail the impairments of social behavior that followed discrete, bilateral lesions of the amygdala. We found, however, that mature rhesus monkeys with bilateral lesions of the amygdala not only were capable of species-typical social behavior, but actually engaged in more affiliative social interactions. The lesioned animals also demonstrated a striking lack of fear of normally fear-inducing stimuli such as replicas of snakes. In a second, ongoing series of studies in the infant rhesus monkey, we are examining whether the amygdala is essential for gaining social knowledge during development. Infant animals that receive bilateral lesions of the amygdala at two weeks of age and are raised by their biological mothers demonstrate all expected social behaviors for their ages. These animals, like the adults, demonstrate a lack of fear of objects such as snakes. However, unlike the adults, they demonstrate more fear when placed into novel social situations. The results from these studies are most consistent with the conclusion that the amygdala is not necessary for species-typical social behavior or for gaining social knowledge during development. We hypothesize that the amygdala is a critical component of a system that evaluates the environment for potential dangers. As such, it has a modulatory role on social behavior-that is, it typically inhibits social interaction with novel conspecifics while they are evaluated as potential adversaries. This perspective predicts that hyperactivity of the amygdala would be associated with increased fear or anxiety and may contribute to disorders such as social phobia.