Oxytocin enhances attention to the eye region in rhesus monkeys

Abstract

Human and non-human primates rely on the ability to perceive and interpret facial expressions to guide effective social interactions. The neuropeptide oxytocin (OT) has been shown to have a critical role in the perception of social cues, and in humans to increase the number of saccades to the eye region. To develop a useful primate model for the effects of OT on information processing, we investigated the influence of OT on gaze behavior during face processing in rhesus macaques. Forty-five minutes after a single intranasal dose of either 24IU OT or saline, monkeys completed a free-viewing task during which they viewed pictures of conspecifics displaying one of three facial expressions (neutral, open-mouth threat or bared-teeth) for 5 s. The monkey was free to explore the face on the screen while the pattern of eye movements was recorded. OT did not increase overall fixations to the face compared to saline. Rather, when monkeys freely viewed conspecific faces, OT increased fixations to the eye region relative to the mouth region. This effect of OT was particularly pronounced when face position on the screen was manipulated so that the eye region was not the first facial feature seen by the monkeys. Together these findings are consistent with prior evidence in humans that intranasal administration of OT specifically enhances visual attention to the eye region compared to other informative facial features, thus validating the use of non-human primates to mechanistically explore how OT modulates social information processing and behavior.

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.…”

“…Scanning began about 40 min after each treatment. A 40-min delay between drug administration and the start of scanning is similar to the timing used in previous monkey and human studies (20)(21)(22)53), as elevations of OT concentration in cerebrospinal fluid have been found ∼40 min after OT administration in monkeys (20,35,36) and humans [AVP, similar to OT with only a two-amino acid difference (54)]. The three monkeys were scanned in two separate sessions per treatment (placebo or OT), resulting in a total of 30 runs (60 condition repetitions) per monkey per treatment.…”

“…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.…”

Enhanced visual exploration for real objects compared to pictures during free viewing in the macaque monkey

“…In visual exploration studies, subjects are generally not rewarded for fixating on particular visual scene elements, to avoid biasing the gaze patterns toward these rewarded locations. A part of the visual exploration literature focuses on gaze patterns during free-viewing of ethologically or socially relevant stimuli, such as faces or body parts of conspecifics or other species (Dal Monte et al, 2014;Ghazanfar et al, 2006;Gothard et al, 2004;Tomonaga, 2009, 2010;Sigala et al, 2011). In this context, gaze patterns are thought to be driven by the need to make predictions about the intentions of other agents (Cannon et al, 2012;Kano and Call, 2014;Southgate et al, 2007), which might be relevant for guiding future behaviors.…”