Social Hierarchy Representation in the Primate Amygdala Reflects the Emotional Ambiguity of Our Social Interactions

Abstract

Group living can help individuals defend against predators and acquire nutrition. However, conflicts between group members can arise (food sharing, mating, etc), requiring individuals to know the social status of each member to promote survival. In our recent paper, we sought to understand how the brain represents the social status of monkeys living in the same colony. Primates learn the social status of their peers through experience, including observation and direct interactions, just like they learn the rewarding or aversive nature of stimuli that predict different types of reinforcement. Group members may thereby be viewed as differing in value. We found in the amygdala, a brain area specialized for emotion, a neural representation of social hierarchy embedded in the same neuronal ensemble engaged in the assignment of motivational significance to previously neutral stimuli. Interestingly, we found 2 subpopulations of amygdala neurons encoding the social status of individuals in an opposite manner. In response to a stimulus, one population encodes similarly appetitive nonsocial images and dominant monkeys as well as aversive nonsocial stimuli and submissive monkeys. The other population encodes the opposite pattern later in time. This mechanism could reflect the emotional ambiguity we face in social situations as each interaction is potentially positive (eg, food access, protection, promotion) or negative (eg, aggression, bullying).