Abstract
The sophisticated analysis of gestures and vocalizations, including assessment of their emotional valence, helps group-living primates efficiently navigate their social environment. Deficits in social information processing and emotion regulation are important components of many human psychiatric illnesses, such as autism, schizophrenia and social anxiety disorder. Analyzing the neurobiology of social information processing and emotion regulation requires a multidisciplinary approach that benefits from comparative studies of humans and animal models. However, many questions remain regarding the relationship between visual attention and arousal while processing social stimuli. Using noninvasive infrared eye-tracking methods, we measured the visual social attention and physiological arousal (pupil diameter) of adult male rhesus monkeys (Macaca mulatta) as they watched social and nonsocial videos. We found that social videos, as compared to nonsocial videos, captured more visual attention, especially if the social signals depicted in the videos were directed towards the subject. Subject-directed social cues and nonsocial nature documentary footage, compared to videos showing conspecifics engaging in naturalistic social interactions, generated larger pupil diameters (indicating heightened sympathetic arousal). These findings indicate that rhesus monkeys will actively engage in watching videos of various kinds. Moreover, infrared eye tracking technology provides a mechanism for sensitively gauging the social interest of presented stimuli. Adult male rhesus monkeys' visual attention and physiological arousal do not always trend in the same direction, and are likely influenced by the content and novelty of a particular visual stimulus. This experiment creates a strong foundation for future experiments that will examine the neural network responsible for social information processing in nonhuman primates. Such studies may provide valuable information relevant to interpreting the neural deficits underlying human psychiatric illnesses such as autism, schizophrenia and social anxiety disorder.
Highlights
Social cognition describes a collection of perceptual, cognitive and regulatory processes that coordinate one’s interactions with others [1,2,3,4,5]
Relative to nature documentary footage, videos showing macaque social signals directed towards the viewer commanded the longest average fixation duration, total fixation duration and average duration of continuous fixation or ‘‘dwell’’ within the video frame
Videos showing conspecifics engaged in naturalistic social interactions resulted in the highest total number of fixations, but videos in this category typically fell between those showing subject-directed social signals or nature documentary footage in fixation duration measures of attention
Summary
Social cognition describes a collection of perceptual, cognitive and regulatory processes that coordinate one’s interactions with others [1,2,3,4,5]. Nonhuman primate studies using selective neurotoxic lesions ([7,8,9,10,11,12]), transient inactivation [13], functional neuroimaging [14,15,16,17,18] and electrophysiological recording techniques [19,20,21,22,23,24,25,26,27,28,29,30,31,32] have implicated the superior temporal cortex, amygdala, orbitofrontal cortex and anterior cingulate cortex in collectively decoding the meaning of social stimuli, orchestrating appropriate social and emotional responses and evaluating outcomes relative to predictions. These findings have largely corroborated data from human functional neuroimaging and lesion studies [33,34,35]
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