Social agent identity cells in the prefrontal cortex of interacting groups of primates

Description 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 Prefrontal neurons in macaques code for the individual and group behavior during giving and receiving in a naturalistic context. INTRODUCTION Social groups play a foundational role in the behavior of many animal species. During group interactions, an individual’s behavior can affect not only the well-being of others but also how others respond in return. Therefore, representing both the identities of others as well as their actions and outcomes is necessary for the ability to interact successfully within groups. Without these combined representations, it would not be possible to engage effectively with others or to understand how one’s actions affect particular group members. It would also not be possible to form mutually beneficial affiliations, avoid exploitation by others, or understand how the behaviors of specific individuals within a group interrelate. RATIONALE Most primates, including humans, live in social groups wherein an individual’s success relies on the ability to interact effectively with others. Rhesus macaques, in particular, are known to form nonkin interactions and long-lasting alliances. They also engage in mutually beneficial behavior based on reciprocity between individual group members. Yet how neurons in the primate brain precisely represent the interactive behavior of groups or resolve the basic problem of coding for multiple agents remains largely unknown. In this study, we developed a three-agent paradigm using small groups of interacting Rhesus macaques in combination with single-neuronal recording and stimulation techniques to begin addressing these questions. RESULTS Groups of adult male rhesus macaques performed a three-agent task in which each individual could offer, in sequence, a food reward to one of the other group members using a rotary table. During these group interactions, we found that the primates reciprocated past offers of reward and retaliated when they did not receive a reward from another. We also observed that the primates formed mutually beneficial affiliations that reflected the reputation and past behavior of other group members. These results, therefore, together suggested that the primates kept track of their interactions with specific individuals within their groups and responded adaptively to the behavior of others. As the primates performed the task, we obtained single-neuronal recordings from the dorsomedial prefrontal cortex (dmPFC; Brodmann’s area 24) in an area proposed to play a role in social behavior and its dysfunction. Collectively, these neurons encoded information about the choices and reward outcomes of different group members, providing, in combination, a highly detailed account of the group’s interactions. These neurons tracked the others’ behaviors across spatial locations, reflecting the social context of the animals’ interactions and the agents involved. They also reliably represented interactions between other individuals, even when those interactions did not involve the recorded animals themselves, thus explicitly linking the identities of others with their specific behaviors. Finally, by following the group’s behavior over time, we find that neurons in the dmPFC reliably tracked prior interactions and integrated information about the past behavior of other agents to influence the animals’ own actions. Modeled together, these neurons reliably predicted the animals’ own upcoming decisions to reciprocate or retaliate in response to the behavior of individual group members. Conversely, disrupting neuronal activity in the dmPFC diminished the animals’ ability to engage in agent-specific behavior and, therefore, their capacity to form mutually favorable interactions. CONCLUSION By following the social behavior of small groups of three rhesus macaques, we find neurons in the dmPFC that code for the agency identity of others and that can therefore link the identities of others with their specific behaviors. By encoding both the current and past actions and outcomes of specific group members, these neuronal ensembles may allow animals to track the behavior of other individuals. In combination with other core areas involved in social cognition, these neurons could form a detailed representation of multiple interactions and together construct a comprehensive “map” of the group’s dynamics. By further integrating information about these dynamics to inform upcoming decisions, these populations could therefore crucially enable the formation of agent-specific interactions necessary for the effective social behavior of groups. A three-agent task in Rhesus macaques reveals a rich representation of group behavior and agent identity in the dmPFC. (Left) Three monkeys sat around a rotary table apparatus that allowed them to allocate food to each other. Simultaneously, we recorded neuronal activity from their dmPFC. (Top right) Individual neurons represented the specific group members offering (actor) and receiving a reward (recipient). (Bottom right) Neurons in the dmPFC collectively encoded detailed information about specific interactions within the group, the directionality of those interactions, the past behavior of other group members, and their influence on the animals? (tm) own decisions. The ability to interact effectively within social groups is essential to primate and human behavior. Yet understanding the neural processes that underlie the interactive behavior of groups or by which neurons solve the basic problem of coding for multiple agents has remained a challenge. By tracking the interindividual dynamics of groups of three interacting rhesus macaques, we discover detailed representations of the groups’ behavior by neurons in the dorsomedial prefrontal cortex, reflecting not only the other agents’ identities but also their specific interactions, social context, actions, and outcomes. We show how these cells collectively represent the interaction between specific group members and their reciprocation, retaliation, and past behaviors. We also show how they influence the animals’ own upcoming decisions and their ability to form beneficial agent-specific interactions. Together, these findings reveal prefrontal neurons that code for the agency identity of others and a cellular mechanism that could support the interactive behavior of social groups.