Oxytocin blunts social vigilance in the rhesus macaque

Abstract

Exogenous application of the neuromodulatory hormone oxytocin (OT) promotes prosocial behavior and can improve social function. It is unclear, however, whether OT promotes prosocial behavior per se, or whether it facilitates social interaction by reducing a state of vigilance toward potential social threats. To disambiguate these two possibilities, we exogenously delivered OT to male rhesus macaques, which have a characteristic pattern of species-typical social vigilance, and examined their performance in three social attention tasks. We first determined that, in the absence of competing task demands or goals, OT increased attention to faces and eyes, as in humans. By contrast, OT reduced species typical social vigilance for unfamiliar, dominant, and emotional faces in two additional tasks. OT eliminated the emergence of a typical state of vigilance when dominant face images were available during a social image choice task. Moreover, OT improved performance on a reward-guided saccade task, despite salient social distractors: OT reduced the interference of unfamiliar faces, particularly emotional ones, when these faces were task irrelevant. Together, these results demonstrate that OT suppresses vigilance toward potential social threats in the rhesus macaque. We hypothesize that a basic role for OT in regulating social vigilance may have facilitated the evolution of prosocial behaviors in humans.attention | primates | face gaze | neuropeptide

Oxytocin modulates fMRI responses to facial expression in macaques

“…Given the similarities between monkeys and humans in the neural circuitry underlying social cognition (19), the rhesus macaque could be an ideal animal model to examine the effects of OT. To date, only a few studies have investigated the behavioral consequences of OT administration in monkeys (20)(21)(22)(23)(24)(25). Consistent with the human literature, these studies have found that intranasal administration of OT affects social behavior and cognition in monkeys, Significance Oxytocin (OT), a mammalian hormone, may serve as a treatment for psychiatric disorders because of its beneficial effect on social behavior.…”

“…This is similar to the dose previously found to affect socially relevant behavior in monkeys (e.g., refs. [20][21][22] and humans (e.g., refs. 8,15,16).…”

“…Thus, the monkey may be an ideal animal model to explore the development of OT-based pharmacologic strategies for treating patients with dysfunctional social behavior. including vicarious as well as self-reinforcement (20), social vigilance (22), socially reinforced learning (26), and attention to facial features and expressions (21,24). However, how OT exerts its effects on brain activity in monkeys remains unclear.…”

Adaptations for social cognition in the primate brain

“…Individuals who increase their number of grooming partners in subsequent months experience a more rapid decrease in fGC levels than females that fail to do so, perhaps because increased grooming allows 'bereaved' females to repair the damage to their grooming network [36]. The link between stress and social attachment may occur, in part, because stress prompts the release of the peptide oxytocin (OT), a hormone that motivates attachment, trust and pair-bonding behaviour (see below) [37][38][39] and suppresses social wariness [40].…”

“…One relatively basic source of variation in cooperative potential is via neuromodulatory effects on neural circuits mediating social bonding [40,108]. For example, OT plays a crucial role in mammalian social behaviour.…”