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.

Keywords: decision; evolution; oxytocin; reward; serotonin.

Fig. 1.

Example neural circuits coopted to serve social functions. (A) Representative brain regions in rhesus macaques whose preexisting functions encompass reward, attention, perception, and executive control. (B) Point of subjective equality (PSE), bias for socially-cued target in terms of foregone juice, after saline or muscimol injections in pSTS. Reproduced from (83) with permission from Oxford University Press. (C) LIP neuron showing firing rate enhancement by observed gaze directed toward the receptive field (RF). (Upper) RF map. (Lower) Neuronal activity as a function of time. Reproduced with permission from ref. .

Fig. 2.

Reward circuits coopted to serve social functions. (A, Left) Firing rates aligned to social image onset for OFC neurons in a social choice task. (Right) Percentage of OFC neurons with activity significantly modulated by social image category (black bar), fluid amount (gray bar), or their interaction (white bar) for three monkeys (M1–M3). Reproduced from (38) with permission from Elsevier. (B, Left) Firing rates of example neurons from each area, aligned to reward delivery. Box color signifies the category to which these neurons belong in the bar graphs. (Right) Proportion of significant neurons from OFC, ACCs, and ACCg using self, other, and shared frames of reference to encode reward outcomes during a reward-allocation task. Horizontal lines indicate significant differences (P < 0.05, χ² test). Reproduced from ref. with permission.

Fig. 3.

Social functions of neuropeptide OT. (A) OT concentration in cerebrospinal fluid (CSF) after inhaling OT (red) or saline (dark gray; *P < 0.05, Welch two-sample t test). Colored outlines on data points indicate animal IDs. (B) Choice preference index for OT (red) and saline (gray) for rewards delivered to: other (recipient) vs. neither, self (actor) vs. other, and self vs. neither in the social reward-allocation task. Data points from self vs. other and self vs. neither are jittered for visibility. Inset shows unjittered data from self vs. other trials. (C) Number of gaze shifts to recipient after reward delivery over the course of each session for other vs. neither choice trials. Reproduced from ref. with permission.

Fig. 4.

Genetic variations in the serotonergic system predict social behavior. (A) Monkeys with a “short” copy of the 5-HTTLPR polymorphism (S/L) show increased pupil dilation to a dominant face (Left), suppressed risk following a dominant face flash (Center), and do not forego juice to view a dominant face (Right). (B) Serotonergic gene profiles predict social network position in free-ranging rhesus macaques. Squares, females; circles, males; lines, presence of a grooming interaction between monkeys. Increasing line thickness indicates frequency of interaction. Node size and position reflect social centrality; largest nodes are the most socially central. Monkeys most central in the network were less likely to carry the minor allele for both the 5-HTTLPR or TPH2 length polymorphisms (gray nodes). A was reproduced from ref. , and B was reproduced from ref. with permission.