The role of dorsal anterior cingulate in cooperative social interactions
Stanford, School of Medicine
While the neuronal circuits underlying perception-action loops of decision making have been studied mostly in the context of an individuals’ internal state, a substantial part of our decisions are made in social contexts which require an additional frame of reference tuned to others’ internal state. A central component of such frame likely draws upon developing a set of models that predict another’s decision based on the recent history of joint interactions. We have recently begun to delineate such neuronal circuits in the non-human primate dorsal anterior cingulate cortex (dACC). In our experiments, pairs of rhesus monkeys play an iterated prisoner’s dilemma game where the monkeys could work together towards a common good or opt to maximize personal outcome over the other’s expense. Obtaining neural recordings from the dACC, we find a class of neurons, which we term “Other-predictive neurons” whose firing rate correlated with the other animal’s upcoming, and yet-unknown decision. These neurons were sensitive to the social context of the interaction and did not encode the monkey’s own decision, expected or received reward (information which we found to be represented by distinct neurons in the dACC). Disruption of dACC activity using microsimulation selectively biased mutually beneficial interactions between the monkeys but, surprisingly, had no effect on their decisions when no net-positive outcome was possible. These result indicate that the cingulate plays an important role in guiding animals’ behavior in social context. In a follow up study we found that similar to humans, inhaled Oxytocin enhances cooperative social behavior in monkeys. Surprisingly, Oxytocin decreased the prevalence of other-predictive neurons in the dACC and weakened the population prediction of the other’s upcoming decision, further corroborating the role of other-predictive neurons. Specifically, neuronal prediction was correlated with the monkeys’ own decision following Oxytocin but not following Saline. These results advance our understanding of the neural basis by which Oxytocin influences interactive social behavior, with implications for the targeted treatment of disorders such as ASD and schizophrenia.