Where and how does the brain code reward during social behavior? Almost all elements of the brain's reward circuit are modulated during social behavior. The striatum in particular is activated by rewards in social situations. However, its role in social behavior is still poorly understood. Here, we attempt to review its participation in social behaviors of different species ranging from voles to humans. Human fMRI experiments show that the striatum is reliably active in relation to others' rewards, to reward inequity and also while learning about social agents. Social contact and rearing conditions have long-lasting effects on behavior, striatal anatomy and physiology in rodents and primates. The striatum also plays a critical role in pair-bond formation and maintenance in monogamous voles. We review recent findings from single neuron recordings showing that the striatum contains cells that link own reward to self or others' actions. These signals might be used to solve the agency-credit assignment problem: the question of whose action was responsible for the reward. Activity in the striatum has been hypothesized to integrate actions with rewards. The picture that emerges from this review is that the striatum is a general-purpose subcortical region capable of integrating social information into coding of social action and reward.

Summary By observing their social partners, primates learn about reward values of objects. Here, we show that monkeys’ amygdala neurons derive object values from observation and use these values to simulate a partner monkey’s decision process. While monkeys alternated making reward-based choices, amygdala neurons encoded object-specific values learned from observation. Dynamic activities converted these values to representations of the recorded monkey’s own choices. Surprisingly, the same activity patterns unfolded spontaneously before partner’s choices in separate neurons, as if these neurons simulated the partner’s decision-making. These “simulation neurons” encoded signatures of mutual-inhibitory decision computation, including value comparisons and value-to-choice conversions, resulting in accurate predictions of partner’s choices. Population decoding identified differential contributions of amygdala subnuclei. Biophysical modeling of amygdala circuits showed that simulation neurons emerge naturally from convergence between object-value neurons and self-other neurons. By simulating decision computations during observation, these neurons could allow primates to reconstruct their social partners’ mental states.

Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific's reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.

A mind’s-eye view of others Social interaction among groups of individuals is a complex proposition. Not only must an animal keep track of various vocalizations and direct interactions in the present but likely also their knowledge of every other individual and their history of interaction with that individual. Two papers begin to unravel the neuronal process by which such complexities are managed (see the Perspective by Sliwa). Báez-Mendoza et al . tracked the interactional dynamics among three Rhesus macaques and found that neurons in the dorsomedial prefrontal cortex represent details of the interaction, such as identity, context, and interaction history. Rose et al . remotely recorded from freely interacting Egyptian fruit bats and similarly found coordinated neural activity among individuals, a relationship between brain activity patterns and social preference, and that single neurons in the prefrontal cortex distinguished between the vocalizations of specific individuals. Together these papers reveal clear evidence for neuronal encoding of social interaction and identity. —SNV

Human social behavior crucially depends on our ability to reason about others. This capacity for ‘theory of mind’ plays a vital role in social cognition because it allows us not only to form a detailed understanding of the hidden thoughts and beliefs of other individuals but to also understand that they may differ from our own 1 – 3 . Although a number of areas in the human brain have been linked to social reasoning 4 , 5 and its disruption across a variety of psychosocial disorders 6 – 8 , the basic cellular mechanisms that underlie human theory of mind remain undefined. Using a rare opportunity to acutely record from single cells in the human dorsomedial prefrontal cortex, we discover neurons that reliably encode information about others’ beliefs across richly varying scenarios and that distinguish self- from other-belief related representations. By further following their encoding dynamics, we show how these cells represent the contents of the other’s beliefs and accurately predict whether they are true or false. We also show how they track inferred beliefs from another’s specific perspective and how their activities relate to behavioral performance. Together, these findings reveal a detailed cellular process in the human dorsomedial prefrontal cortex for representing another’s beliefs and identify candidate neurons that could support theory of mind.