Cortical representation of group social communication in bats

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 A dedicated intra- and interbrain neural repertoire underlies group social communication in Egyptian fruit bats. INTRODUCTION Many animals live and interact as part of social groups. Social groups present unique advantages to their members, but also necessitate viable modes of communication between individuals, such as vocalization. Yet the neural mechanisms that support group social-vocal communication remain largely unknown. This is because most previous studies have focused on only one side of communication at a time, have measured neural activity in only one brain at a time, and were conducted outside the group social setting. This limited studies of key aspects of group social communication, such as the neural representation of self versus others, individual identity, and the influence of social relationships and context on both inter- and intrabrain activity patterns. Therefore, a major knowledge gap exists between the ethology of group social communication and the study of its neurophysiological basis. RATIONALE Egyptian fruit bats live in large groups where individuals form long-lasting social relationships. Communication within these groups occurs through vocalizations that carry socially relevant information relating to individual identity, context, and social relationships. Using simultaneous multi-animal wireless neurophysiological recordings and novel behavioral monitoring techniques, we set out to study the neural basis of social-vocal communication in a group. We focused on the frontal cortex, an area shown to be involved in aspects of vocal and social behaviors across a variety of species. RESULTS We allowed groups of bats to interact freely and vocalize as they naturally would when clustered together in the wild. During freely occurring social-vocal interactions, we observed two main patterns of neural activity, one within individual brains and one shared across the brains of group members. Within individual brains, we observed that single-neuron activity could be used to distinguish between vocalizations made by oneself and others. Moreover, the identity of the vocalizing individual could be decoded from the activity of single neurons, beyond what would be expected on the basis of acoustic differences between the vocalizing bats. Across brains, we found that vocalizations elicited synchrony in the power of the high-frequency local field potential between group members. These synchronization patterns were bidirectional and remained stable over weeks of recording. To further dissociate the sensorimotor aspects of the vocal interactions from the social-communicative aspects, we trained bats to vocalize for reward in a setting where vocalizations would not otherwise occur. We found that during trained vocalizations, single-neuron activity was restructured and interbrain shared activity patterns were abolished. Finally, we found that both the intra- and interbrain activity patterns were modulated by the social preferences of individual group members, such that bats preferring to spend more time with others elicited stronger neural identity representation and higher levels of interbrain synchrony. CONCLUSION By studying cortical activity in groups of highly social mammals, we uncovered a dedicated neural repertoire for group social communication. We also found that both intra- and interbrain activity patterns were modulated by social context and individual social preferences. Our findings further underscore the benefits of studying neural circuits in specialized model systems while considering ethologically relevant aspects of their behavior. A neural repertoire for communication in social groups. (A) We wirelessly recorded single-neuron activity and local field potential (LFP) from the frontal cortices of multiple bats in a group as they freely engaged in social-vocal interactions. (B) Single-neuron activity could be used to distinguish between vocalizations made by oneself (self-responsive) and other bats (other-responsive). The activity of identity-selective neurons could be used to further distinguish between the vocalizations of individual bats. (C) High-frequency LFP power became transiently correlated across the brains of group members during vocal interactions. (D) By comparing spontaneously occurring vocalizations to vocalizations made for reward, we found that single-neuron activity is restructured across contexts and that interbrain correlation is absent during trained vocalizations. (E) Vocalizations produced by bats preferring to spend more time with other group members elicited more accurate single-neuron identity selectivity and higher levels of interbrain correlation. Social interactions occur in group settings and are mediated by communication signals that are exchanged between individuals, often using vocalizations. The neural representation of group social communication remains largely unexplored. We conducted simultaneous wireless electrophysiological recordings from the frontal cortices of groups of Egyptian fruit bats engaged in both spontaneous and task-induced vocal interactions. We found that the activity of single neurons distinguished between vocalizations produced by self and by others, as well as among specific individuals. Coordinated neural activity among group members exhibited stable bidirectional interbrain correlation patterns specific to spontaneous communicative interactions. Tracking social and spatial arrangements within a group revealed a relationship between social preferences and intra- and interbrain activity patterns. Combined, these findings reveal a dedicated neural repertoire for group social communication within and across the brains of freely communicating groups of bats.