Impact of amygdala, orbital frontal, or hippocampal lesions on threat avoidance and emotional reactivity in nonhuman primates.

The authors measured the effects of bilateral amygdaloid, orbital frontal, or hippocampal lesions on emotional reactivity and passive avoidance in rhesus monkeys (Macaca mulatta). Animals were presented with 8 neutral or 8 aversive objects, each paired with a highly preferred food reward. Sham-operated control animals displayed heightened defensive behaviors and typically would not approach or retrieve the food when paired with a potential predator (coiled rubber snake), 2 conditioned aversive stimuli for laboratory-housed monkeys (a capture net and leather handling gloves), and 1 object displaying a threatening social signal (direct eye contact from a human-like doll). Animals with amygdala lesions, but not hippocampal or orbital frontal lesions, showed less tension-related behaviors and diminished passive avoidance of the rubber snake and its matched neutral item (a coiled piece of hose) relative to control animals. All operated groups displayed normal patterns of behavior toward conditioned and socially aversive objects. These results expand our understanding of how the primate brain evaluates reward and threat, and indicate a highly specialized role for the amygdala in mediating passive avoidance and emotional reactivity to potentially life-threatening stimuli.