Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques ( Macaca mulatta )

Abstract

People attend not only to their own experiences, but also to the experiences of those around them. Such social awareness profoundly influences human behavior by enabling observational learning, as well as by motivating cooperation, charity, empathy, and spite. Oxytocin (OT), a neurosecretory hormone synthesized by hypothalamic neurons in the mammalian brain, can enhance affiliation or boost exclusion in different species in distinct contexts, belying any simple mechanistic neural model. Here we show that inhaled OT penetrates the CNS and subsequently enhances the sensitivity of rhesus macaques to rewards occurring to others as well as themselves. Roughly 2 h after inhaling OT, monkeys increased the frequency of prosocial choices associated with reward to another monkey when the alternative was to reward no one. OT also increased attention to the recipient monkey as well as the time it took to render such a decision. In contrast, within the first 2 h following inhalation, OT increased selfish choices associated with delivery of reward to self over a reward to the other monkey, without affecting attention or decision latency. Despite the differences in species typical social behavior, exogenous, inhaled OT causally promotes social donation behavior in rhesus monkeys, as it does in more egalitarian and monogamous ones, like prairie voles and humans, when there is no perceived cost to self. These findings potentially implicate shared neural mechanisms. O xytocin (OT) (1) is a mammalian neurosecretory hormone, synthesized by hypothalamic neurons, which regulates the hypothalamic-pituitary-adrenal axis (2). The most well-understood role of OT in mammals is in female reproduction, with peripheral OT influencing parturition and lactation (3), and central OT affecting mother-offspring bonding and recognition (4, 5). More recently, OT has been found to influence nonparental social behavior in a species-specific manner. For example, OT promotes pair-bonding between males and females in monogamous prairie voles (Microtus ochrogaster) (6, 7) but can also increase aggression (i.e., mate-guarding behavior) and decrease social interaction among females after brief exposure to a male (8). In humans, OT also influences more complex forms of social behavior and cognition (9-14). For example, inhaled OT enhances trusting behavior toward other individuals in economic games, potentially by suppressing aversion to betrayal risk (15), and promotes cooperation within groups (16). However, inhaled OT also provokes cultural and racial biases (17). OT inhalation also enhances sensitivity to the experiences of others by promoting vicarious reward and empathic pain (10,18,19). Recently, OT-mediated processes have been implicated in disorders attended by dysfunctional social behavior, including autism, fragile X syndrome, and schizophrenia (19)(20)(21)(22). Notably, OT treatment improves social skills in individuals with autism (21, 23, 24), a spectrum of disorders with marked deficits in sensitivity to what happens to others, including impai...

Oxytocin blunts social vigilance in the rhesus macaque

“…As reported previously in humans (8,10,11), we found that OT increased gaze to the eye regions of photos of other monkeys. However, in contrast to the hypothesis that OT generally heightens social attention (4,5,(8)(9)(10), OT reduced species-typical vigilance for unfamiliar, emotional, and dominant faces in two additional experiments. In a social image choice task in which monkeys chose between symbolic targets to view or not view social images, OT prevented the emergence of a typical vigilance state for faces of dominant males.…”

“…Reduced social vigilance may contribute to the increase in prosocial behavior previously observed following OT treatment (4,5). By reducing the typical state of vigilance for social threats, OT may impede the acquisition of information about negative social cues, thereby permitting, rather than promoting prosocial behaviors that might otherwise be inhibited by those cues.…”

“…In squirrel monkeys, for example, intracerebral OT administration increases male-male aggression in dominant individuals, but also social contact in subordinate males (3). In rhesus macaques, intranasal OT increases the number of rewards a monkey chooses to deliver to another monkey when there is no cost to himself, but also enhances a selfish bias when there is an option to reward himself (4). These complex effects of OT are also observed in humans (5).…”

“…Inhaled OT increases gaze toward the eye region of faces in humans (8,10,11) and increases the frequency and duration that rhesus macaques look at other monkeys (4). However, OT may not generally enhance social attention, but instead may bias social attention.…”

“…One possible mechanistic explanation for these complex effects is that OT may alter social attention, which would necessarily adjust the information available for social perception and decision making (4,5,(8)(9)(10). Inhaled OT increases gaze toward the eye region of faces in humans (8,10,11) and increases the frequency and duration that rhesus macaques look at other monkeys (4).…”