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.

Fig. 1.

Reward allocation task. (A) Experimental setup. (B) Trial sequence. Choice (Upper) and cued (Lower) trials were randomly interleaved. The eye-gaze cartoons specify the task intervals during which the donors could potentially look at the recipient monkey. MT, movement time; RT, reaction time. (C) Stimuli associated with different reward outcomes to donors and recipient, shown separately for the two donors. (D) OT concentration in the CSF after intranasal OT (in red) or saline (dark gray). *P < 0.05, Welch two-sample t test. Colored outlines on the datapoints represent animal identities.

Fig. 2.

Intranasal OT promotes both vicarious and self reinforcement. Choice preference index (moving averages of 200 trials per session, 50-trial step) for OT (red) and saline (gray) across all reward options (other vs. neither, self vs. other, and self vs. neither). Datapoints from self vs. other and self vs. neither are jittered along the ordinate for visibility. (Inset) Unjittered and magnified data from self vs. other trials. Data from self vs. neither trials were effectively overlapping between the OT and saline conditions, and therefore not shown in an unjittered format. OT, 12 sessions; saline, 10 sessions. Lines show linear regression on other vs. neither trials.

Fig. 3.

Intranasal OT enhances attention to the recipient monkey and increases the deliberation time for making donation decisions. (A) Gaze to the face of the other monkey after reward delivery. (Left) Percentages of gaze shifts to the recipient monkey on choice trials (Upper) and cued trials (Lower). (Right) Number of gaze shifts over the course of each day session for other vs. neither choice trials (moving averages of 200 trials per session, 50-trial step). Lines through the datapoints show linear regressions. (B) Response times, measured as saccade onset times following target onset (ms). (C) OT reduced choice avoidance [i.e., declining to choose by breaking fixation upon target onset (such as, reward options), which, in the task resulted in a time out for 5 s]. *P < 0.05, Welch two-sample t test.