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...

Summary Whether driving a car, shopping for food, or paying attention in a classroom of boisterous teenagers, it’s often hard to maintain focus on goals in the face of distraction. Brain imaging studies in humans implicate the dorsal anterior cingulate cortex (dACC) in regulating the conflict between goals and distractors. Here we show for the first time that single dACC neurons signal conflict between task goals and distractors in the rhesus macaque, particularly for biologically-relevant social stimuli. For some neurons, task conflict signals predicted subsequent changes in pupil size—a peripheral index of arousal linked to noradrenergic tone—associated with reduced distractor interference. dACC neurons also responded to errors and these signals predicted adjustments in pupil size. These findings provide the first neurophysiological endorsement of the hypothesis that dACC regulates conflict, in part, via modulation of pupil-linked processes such as arousal.

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