Social monitoring of actions in the macaque frontopolar cortex.

Abstract

The frontopolar cortex (FPC) of primates appeared as a main innovation in the evolution of anthropoid primates and it has been placed at the top of the prefrontal hierarchy. The only study to date that investigated the activity of FPC neurons in monkeys performing a cognitive task suggested that these cells were involved in the monitoring of self-generated actions. We recorded the activity of neurons in the FPCs of two rhesus monkeys while they performed a social variant of a nonmatch-to-goal task that required monitoring the actions of a human or computer agent. We discovered that the role of FPC neurons extends beyond self-generated actions to include monitoring others' actions. Their monitoring activity was very specific. First, neurons in the FPC encoded the spatial position of the target but not its object features. Second, a dedicated representation of the human agent actions was tied to the time of target acquisition, while it was reduced or absent in the successive epochs of the trial. Finally, this other-specific neural substrate did not emerge during the interaction with a virtual agent such as the computer. These results provide a new perspective on the functions of a uniquely primate brain area, suggesting that FPC might play an important role in social behaviors.