Pragmatic representations of self- and others’ action in the monkey putamen

Abstract

Abstract Social coordination in primates relies on parieto-frontal networks encoding self- and others’ actions. These areas send convergent projections to the putamen, but its role in representing self- and others’ actions remains unknown. We recorded neuronal activity from anatomically characterized putamen regions of two male macaques during a Mutual Action Task (MAT), where a monkey and a human took turns grasping a multi-affordance object based on sensory cues. Cortico-striatal synaptic input, indexed by local field potentials, mirrored known cortical dynamics during sensory instructions and movement, while single neurons selectively encoded the monkey’s action, the human’s action, or both. Grip type was encoded only during the monkey’s trials. Viewing the partner’s action was neither necessary nor sufficient, as neurons fired even when it occurred in darkness but not when viewed through a transparent barrier. Thus, the possibility for actual interaction characterizes the pragmatic role of the putamen in gating cortical representations of self- and other’s actions in social contexts.