Oxytocin and testosterone administration amplify viewing preferences for sexual images in male rhesus macaques

Abstract

Social stimuli, like faces, and sexual stimuli, like genitalia, spontaneously attract visual attention in both human and non-human primates. Social orienting behaviour is thought to be modulated by neuropeptides as well as sex hormones. Using a free viewing task in which paired images of monkey faces and anogenital regions were presented simultaneously, we found that male rhesus macaques overwhelmingly preferred to view images of anogenital regions over faces. They were more likely to make an initial gaze shift towards, and spent more time viewing, anogenital regions compared with faces, and this preference was accompanied by relatively constricted pupils. On face images, monkeys mostly fixated on the forehead and eyes. These viewing preferences were found for images of both males and females. Both oxytocin (OT), a neuropeptide linked to social bonding and affiliation, and testosterone (TE), a sex hormone implicated in mating and aggression, amplified the pre-existing orienting bias for female genitalia over female faces; neither treatment altered the viewing preference for male anogenital regions over male faces. Testosterone but not OT increased the probability of monkeys making the first gaze shift towards female anogenital rather than face pictures, with the strongest effects on anogenital images of young and unfamiliar females. Finally, both OT and TE promoted viewing of the forehead region of both female and male faces, which display sexual skins, but decreased the relative salience of the eyes of older males. Together, these results invite the hypothesis that both OT and TE regulate reproductive behaviours by acting as a gain control on the visual orienting network to increase attention to mating-relevant signals in the environment. This article is part of the theme issue ‘Interplays between oxytocin and other neuromodulators in shaping complex social behaviours’.

The interplay of oxytocin and sex hormones

“…Moreover, emerging evidence emphasizes the importance of the interaction between oxytocin and sex hormones in supporting a plethora of cognitive, behavioral, and physiological functions. Findings suggest that this interaction is involved in regulating sexual behavior (Jiang et al, 2022) or parental behavior (Gordon et al, 2017) to facilitate reproduction. Others propose that the interaction of sex hormones and oxytocin modulates well-being (Love, 2018) and sociality (Schneider et al, 2021) to aid survival.…”

“…This opposing effect of testosterone and oxytocin in reproductive behaviors appears to be inconsistent across species. For example, in rhesus macaques both oxytocin and testosterone increased gaze towards sexual stimuli in macaques compared to the baseline (Jiang et al, 2022). Changes in hippocampal volume in first-time fathers has also been associated with prenatal oxytocin levels and postpartum testosterone levels, which may contribute to improved parent-child bonding (Saxbe et al, 2023).…”

The Roles of Androgens in Humans: Biology, Metabolic Regulation and Health

“…T is necessary for mating and the maintenance of a sexual/affective relationship for both sexes [ 272 ]. T activates mating relationships [ 273 ] through complex mechanisms in which cortisol [ 274 ] and reward systems, such as endorphins [ 275 ] and oxytocin [ 276 ], play important roles. The settling of durable relationships result in a decrease in T [ 277 ] and increase in oxytocin [ 278 , 279 ] levels in males.…”

Oxytocin does not stand alone

“…Adding to this understanding, Jiang et al . [ 62 ] examined how both oxytocin and testosterone modulated the gaze of non-human primates when shown conspecific social and sexual images. Both oxytocin and testosterone increased the innate bias for gaze on female genitalia over female faces and promoted viewing of the forehead region where rhesus monkeys ( Macaca mulatta ) display sexual skin.…”