150w): 2Here we demonstrate that during strategic gameplay monkeys behave as if they reason 4 recursively about other individuals' beliefs and desires in order to predict their choices and to guide their own actions, especially the decision to cooperate. Neurons in mid superior temporal 6 sulcus (mSTS), the putative homolog of the human temporo-parietal junction (TPJ), signal abstract non-perceptual social information, including payoffs, intentions, and outcomes, and 8 further distinguish between social and nonsocial agents while monkeys play the game. We demonstrate for the first time that a subpopulation of these neurons selectively signals 10 cooperatively obtained rewards. Neurons in the anterior cingulate gyrus (ACCg), an area implicated in vicarious reinforcement and empathy, do not distinguish agency and as a 12population carry less information about strategic variables. These findings suggest the capacity to mentalize has deep roots in the strategic social behavior of primates, and endorse mSTS as the 14 evolutionary wellspring of these functions. 16
Main: 18Both emotional and cognitive mechanisms shape the decisions people make when they interact 20 with others 1,2 . Specifically, vicarious feelings of reward or pain experienced by another, often termed empathy, can provoke prosocial actions 3 . Strategic reasoning about the beliefs, desires, 22and goals of another individual, a process referred to as mentalizing or theory of mind, guides the decision to cooperate with or betray a partner 4,5 . These two processes interact as well; 24 manipulations that increase empathy enhance cooperation 6 . Two separate but interacting brain systems appear to support empathy and mentalizing during social decisions 7 . In humans, 26 empathy and vicarious experience evoke hemodynamic activity in anterior cingulate gyrus (ACCg), anterior insula, and amygdala, and neurons in primate ACCg and amygdala signal 28vicarious rewards delivered to other monkeys 8,9 . By contrast, thinking about the beliefs, desires, or goals of others evokes hemodynamic activity in the dorsomedial prefrontal cortex and 30 temporo-parietal junction (TPJ) in humans 7,10-12 . The neuronal mechanisms underlying such mentalizing-related brain activity, however, remain poorly understood in part due to the 32 difficulty of eliciting recursive social reasoning in primates or other animals in which neuronal activity can be studied directly (but see Haroush 13 ) as well as the lack of neurophysiological or 34histological evidence for a TPJ homolog in nonhuman primates 14,15 . 36To address this gap, we trained monkeys to play a version of the classic "chicken" game from behavioral economics 16 . We also recorded spiking activity of 448 neurons in the middle 38 superior temporal sulcus (mSTS), a brain area known to encode perceptual social information like faces 17,18 and recently proposed as the primate homolog of TPJ based on MRI-based 40 functional connectivity 15 . For comparison, we recorded spiking activity of 528 neurons in ACCg, an area strongly l...