Social state representation in prefrontal cortex

Abstract

One of the cardinal mental faculties of humans and other primates is social brain function, the collective name assigned to the distributed system of social cognitive processes that orchestrate our sophisticated adaptive social behavior. These must include processes for recognizing current social context and maintaining an internal representation of the current social state as a reference for decision-making. But how and where the brain processes such social-state information is unknown. To home in on the neural substrates of social-state representation, the activity of 196 prefrontal (PFC) neurons was recorded from two monkeys simultaneously during a food-grab task under varying social conditions. Of PFC neurons, 39% showed activity modulation during movement-free periods and seemed to be representing current social state. The direction of modulation was opposite between the dominant and submissive monkeys: During social engagement, PFC activity increased in the dominant monkey and was suppressed in the submissive monkey. The modulation was consistently observed in additional PFC neurons (27/72) in additional pairings with two other monkeys. Notably, PFC activity in one formerly submissive monkey switched to dominant modulation mode when he was paired with a new monkey of lower social status. These findings suggest that PFC, as part of a larger social brain network, maintains a multistate classification of social context for use as a behavioral reference for social decision-making.

Acknowledgements

We thank Kenji Matsumoto for his valuable comments and T. Notoya and K. Takenaka for their technical assistance. This research was supported by a Grant-in-Aid for Scientific Research on Priority Areas (Integrative Brain Research) from the MEXT of Japan (17021048), a Grant-in-Aid for Scientific Research on Priority Areas (Mobiligence) from the MEXT of Japan (18047029), and the 2006 Riken Strategic Programs for R&D (President's Discretionary Fund).