Neuroethology of primate social behavior

Abstract

A neuroethological approach to human and nonhuman primate behavior and cognition predicts biological specializations for social life. Evidence reviewed here indicates that ancestral mechanisms are often duplicated, repurposed, and differentially regulated to support social behavior. Focusing on recent research from nonhuman primates, we describe how the primate brain might implement social functions by coopting and extending preexisting mechanisms that previously supported nonsocial functions. This approach reveals that highly specialized mechanisms have evolved to decipher the immediate social context, and parallel circuits have evolved to translate social perceptual signals and nonsocial perceptual signals into partially integrated social and nonsocial motivational signals, which together inform general-purpose mechanisms that command behavior. Differences in social behavior between species, as well as between individuals within a species, result in part from neuromodulatory regulation of these neural circuits, which itself appears to be under partial genetic control. Ultimately, intraspecific variation in social behavior has differential fitness consequences, providing fundamental building blocks of natural selection. Our review suggests that the neuroethological approach to primate behavior may provide unique insights into human psychopathology.decision | evolution | reward | serotonin | oxytocin S ensitivity and responsiveness to information about others is critical for human health (1, 2), survival (3), and even financial success (4). To navigate our social worlds, we track the behavior of others and form models of their intentions and emotional states, we actively seek out and exchange information about others, and we flexibly alter our behavior in response to what we know about others. These faculties are so important to human behavior that their disruption constitutes psychopathology (5, 6). These specializations for social behavior reflect a rich evolutionary heritage of adaptation to group life (7-9). Like humans, many nonhuman primates also live in large groups characterized by patterns of social behaviors like grooming, imitative and cooperative foraging, differentiated affiliative relationships, ritualized courtship and mating behavior, and competitive interactions structured by social dominance (10, 11). Not surprisingly, the ability to deftly navigate the social environment has observable consequences for reproductive success in some nonhuman primates (12). Evolutionary Perspective on Social BehaviorSocial behavior places strong and unique demands on the nervous system. Across primate species, group size (a potential proxy of social complexity) is correlated with forebrain volume, after correcting for body size (9). Additional brain tissue beyond that required to maintain a body of a particular size is costly, in both developmental complexity and metabolic demands (7, 13-15). Indeed, social complexity and the elaboration of neural mechanisms to support it are associated with diets high in dependa...

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“…R. Soc. B 370: 20150014 by infants [13,42] (table 1). While OT has similar impacts on lactation and behaviour across many mammals, human and great ape altriciality coupled with relatively high dependency loads may have placed additional selective pressures on proximate mechanisms that modulated maternal behaviour, in particular tolerance to a long period of offspring contact and (multiple) dependence.…”

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Neural mechanisms of social decision-making in the primate amygdala

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