Simultaneous intracranial recordings of interacting brains reveal neurocognitive dynamics of human cooperation

Abstract

Cooperative interactions profoundly shape individual and collective behaviors of social animals. Successful cooperation requires coordinated efforts by cooperators toward collective goals. However, the underlying behavioral dynamics and neuronal mechanisms within and between cooperating brains remain largely unknown. We recorded intracranial electrophysiological signals from human pairs engaged in a cooperation game. We show that teammate coordination and goal pursuit make distinct contributions to the behavioral cooperation dynamics. Increases and decreases in high-gamma activity in the temporoparietal junction (TPJ) and amygdala distinguish between establishing and maintaining cooperation and forecast transitions between these two states. High-gamma activity from distinct neuronal populations encodes teammate coordination and goal pursuit motives, with populations of TPJ neurons preferentially tracking dominant motives of different cooperation states. Across cooperating brains, high-gamma activity in the TPJ and amygdala synchronizes in a state-dependent manner that predicts how well cooperators coordinate. These findings provide fine-grained understandings of human cooperation dynamics as a state-dependent process with distinctive neurocognitive profiles of each state.