The Social Switchboard: Context and Rank Shapes Behavioural and Neural Responses During Macaque Decision-Making

Abstract

Key PointsO_LISociality influences ethologically important decisions and demand a high level of cognitive sophistication C_LIO_LIWe used a novel decision making task with 6 macaques where social hierarchy could be tested across social audience, coaction, envy, altruism, cooperation & competition contexts. C_LIO_LISubjects decision making performance was significantly modulated by context and social rank, reflected by their social eye gaze patterns. C_LIO_LIThere were significant differences in fronto-parietal brain regions as the social context changed C_LI Social interactions shape many of our most ethologically relevant decisions and require considerable cognitive sophistication. Factors such as immediate needs, social bonds, hierarchical status, and reciprocity norms impact decision-making. Yet most laboratory paradigms examine individuals in isolation. We developed a face-to-face cognitive testing platform using a transparent touchscreen that allowed pairs of adult male Macaca fascicularis (n = 6) with established dominance relationships to perform a decision-making task across six social contexts: audience, co-action, envy, cooperation, competition, and altruism. We recorded eye movements simultaneously from both subjects (gaze position and pupil diameter), synchronised behavioural video, and task performance. Across social contexts, macaques performed better in the presence of a conspecific than when tested alone, but performance declined under altruistic and competitive conditions. Dominance substantially modulated motivation: dominant subjects were less willing to engage when rewards were shared (envy), when only the partner was rewarded (altruism), or when contingent action with a subordinate was required (cooperation). Eye-tracking revealed greater pre-choice arousal and social attention during social sessions, indexed by larger pupils, longer fixations on the partners face, and more saccades before--but not during or after--choices. Pupil dilation was larger in dyads where both individuals were dominant than in dyads where one was subordinate. Finally, noninvasive functional near-infrared spectroscopy (fNIRS) showed increased cortical engagement relative to baseline in audience, altruism, competition, and cooperation conditions. These findings demonstrate that social context and hierarchical dominance systematically shape choices, attentional allocation, autonomic arousal, and cortical engagement in macaques, and provide a tractable platform for further dissecting the neural bases of contextual social decisionmaking.