Intranasal oxytocin selectively attenuates rhesus monkeys’ attention to negative facial expressions

Abstract

Intranasal oxytocin (IN-OT) modulates social perception and cognition in humans and could be an effective pharmacotherapy for treating social impairments associated with neuropsychiatric disorders, like autism. However, it is unknown how IN-OT modulates social cognition, its effect after repeated use, or its impact on the developing brain. Animal models are urgently needed. This study examined the effect of IN-OT on social perception in monkeys using tasks that reveal some of the social impairments seen in autism. Six rhesus macaques (Macaca mulatta, 4 males) received a 48 IU dose of OT or saline placebo using a pediatric nebulizer. An hour later, they performed a computerized task (the dot-probe task) to measure their attentional bias to social, emotional, and nonsocial images. Results showed that IN-OT significantly reduced monkeys’ attention to negative facial expressions, but not neutral faces or clip art images and, additionally, showed a trend to enhance monkeys’ attention to direct versus averted gaze faces. This study is the first to demonstrate an effect of IN-OT on social perception in monkeys, IN-OT selectively reduced monkey’s attention to negative facial expressions, but not neutral social or nonsocial images. These findings complement several reports in humans showing that IN-OT reduces the aversive quality of social images suggesting that, like humans, monkey social perception is mediated by the oxytocinergic system. Importantly, these results in monkeys suggest that IN-OT does not dampen the emotional salience of social stimuli, but rather acts to affect the evaluation of emotional images during the early stages of information processing.

Oxytocin blunts social vigilance in the rhesus macaque

“…Experiment 3 replicates observations in unrestrained rhesus macaques that intranasal OT blunts orienting toward unfamiliar, emotionally expressive faces displayed in the context of a dotprobe task (24). The present results extend the previous report in two significant ways.…”

“…Our findings suggest that positive social interactions can reduce social vigilance via OT release, thereby freeing attentional resources for other social and goal-directed behaviors. Thus, our findings resonate with the idea that OT biases global social processes away from negative information and toward positive information (24,26). For example, OT promotes positive implicit associations with in-group members, but has mixed effects on associations with out-group members (7).…”

Oxytocin modulates fMRI responses to facial expression in macaques

“…Consistent with our findings, a previous study found that intranasally administered OT reduced monkeys' attention to negative facial expressions (fear grin and open-mouth threat), but not to neutral or nonsocial stimuli (24).…”

“…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.…”

“…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.…”