Dynamic tracking of social variables in simultaneous brain recordings from socially interacting monkeys

ABSTRACT Primates are deeply social, but understanding the neural basis has been challenging since it has previously only been possible to record from single monkeys interacting with a social partner. Here, we performed simultaneous wireless neural recordings from two macaque monkeys interacting socially in a natural, unconstrained setting. Neural activity in each monkey encoded key social variables such as allogrooming state, partner identity and joint movements. Interestingly, neurons in the high-level visual cortex of each monkey continuously tracked a social favor signal, i.e. net duration of allogrooming given versus received, providing a neural basis for grooming reciprocity. In each monkey, neural activity was predicted better by his partner’s joints and neural activity, particularly while giving compared to receiving grooming. Thus, the receiver of grooming drove the social interaction, not the groomer. Taken together, our findings elucidate the rich and dynamic neural basis of primate social interactions in an ecologically valid setting. SIGNIFICANCE STATEMENT Primates are deeply social, but understanding this requires recording neural activity simultaneously and unobtrusively from two animals without constraints. Here, we performed the first-ever simultaneous wireless brain recordings from two monkeys socially interacting in a natural setting. We found that both monkeys’ brains tracked important social variables, such as a social favor signal as well as their partner’s identity and movements. Interestingly, the receiver of grooming seemed to drive the social interaction, as evidenced by referential gestures during behavior, stronger tracking of the grooming receivers’ joints and stronger prediction of the groomer’s brain activity by the receiver’s brain activity. Our results represent an important first step towards understanding primate social interactions in an ecologically valid setting.