PhilTransData.zip from Oxytocin and testosterone administration amplify viewing preferences for sexual images in male rhesus macaques

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’.

诸如面孔这类社会刺激，以及生殖器这类性刺激，均会在人类与非人灵长类动物中自发吸引视觉注意力。学界普遍认为，社会定向行为会受到神经肽与性激素的共同调控。我们采用同时呈现猴面孔与肛生殖区（anogenital regions）成对图像的自由观看任务（free viewing task），发现雄性恒河猴（rhesus macaques）压倒性地更偏好观看肛生殖区图像而非面孔图像：相较于面孔，它们更倾向于首次将目光扫视至肛生殖区，且在该区域的注视时长更长，这一偏好同时伴随瞳孔相对收缩的生理现象。在面孔图像中，猴类大多会将注视点落在前额与眼部。这类观看偏好同时存在于雄性与雌性的图像中。催产素（oxytocin, OT）作为与社会联结和亲和行为相关的神经肽，以及睾酮（testosterone, TE）作为与交配和攻击行为相关的性激素，均会放大既有的定向偏好——即雌性肛生殖区相较于雌性面孔的注视偏好；但两种药物处理均未改变雄性肛生殖区相较于雄性面孔的观看偏好。相较于催产素，睾酮（而非催产素）提升了猴类首次将目光扫视至雌性肛生殖区而非雌性面孔的概率，该效应在年轻且陌生的雌性肛生殖区图像上表现最为显著。最后，催产素与睾酮均会促使猴类注视展示性皮肤特征的雌雄面孔前额区域，同时降低老年雄性面孔眼部的相对显著性。综合上述结果，我们提出假说：催产素与睾酮均通过对视觉定向网络（visual orienting network）施加增益调控，提升个体对环境中与交配相关的信号的注意力，从而调节生殖行为。本文属于"催产素与其他神经调节剂在塑造复杂社会行为中的交互作用"主题特刊的组成部分。