From Behavior to Neural Circuits: A Multi-Method Investigation of Social Decision-Making in Macaques

Most neurocognitive studies of decision-making examine isolated subjects, yet our most consequential choices are made in a social world governed by various contexts. To bridge this gap, we developed a novel head-free cognitive testing platform that facilitates more natural, face-to-face interactions for pairs of male Macaca fascicularis (n=6) with established dominance relationships. This system allows us to present a classic decision-making task across six ethologically relevant social contexts: audience, co-action, envy, cooperation, competition, and altruism. Using this paradigm, we conducted a comprehensive multi-modal study. We recorded simultaneous eye movements (gaze position and pupil diameter) from both subjects, synchronized behavioral video monitoring, and task performance. This revealed that while macaques generally performed better in the presence of a conspecific, performance declined under altruistic and competitive conditions. Dominance substantially modulated motivation: dominant subjects disengaged when rewards were shared, when only the partner was rewarded, or when contingent action with a subordinate was required. Eye-tracking quantified the cognitive load of social processing, showing greater pre-choice arousal and social attention during social sessions—indexed by larger pupils, longer fixations on the partner’s face, and more saccades before choices. Complementary noninvasive functional near-infrared spectroscopy (fNIRS) showed increased cortical engagement in audience, altruism, competition, and cooperation contexts. Their heart rate affect by dominance and context of the task as well. These findings demonstrate that social context and hierarchical dominance systematically shape choices, attentional allocation, autonomic arousal, and cortical engagement. Our work provides a uniquely tractable and ethologically valid platform to dissect the neural bases of contextual social decision-making. Building on this foundational behavioral and physiological characterization, we have now initiated a critical investigation into neural circuits. This integrative, multi-level approach is essential for advancing models of social cognition with direct relevance to understanding human social behavior and its dysfunction in psychiatric disorders.