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How do the brains of bats manage complex group social interactions

Living as part of a social group has great advantages for individuals but it also requires the ability to communicate effectively with other group members. It is still unclear how brains manage to achieve this complex task and how differences between individuals are represented in the brains of other group members. By simultaneously recording from the cortex of several group members of the highly social Egyptian fruit bat, as they freely vocally interact with each other, we found a dedicated neural repertoire for group social interaction within and across the brains of group members.

Group living is key in the lives of many animals yet it necessities viable modes of communication between group members to facilitate successful social interactions. Little is known about how the brains of mammals can support the complex social vocal communication that group living requires. 

Example of bats clustered together in a group in the recording enclosure (right). We wirelessly recorded single neuron and field potential from 3-4 group members simultaneously as they freely communicated using vocalization (left illustration).

To address this challenge, we utilized the highly social mammal, the Egyptian fruit bat (Rousettus aegyptus) to study how the cortex represents social interactions within and across the brains of group members. These mammals have long lives (up to 25 years) and form tight social groups that can range from hundreds to thousands of individuals. They have a rich vocal repertoire and use vocalizations exclusively when in close contact interaction with conspecifics. These behavioral features enabled us to investigate how the brains of bats process these social-vocal interactions in the group setting. We thus developed both on-animal vocalization detectors as well as multi-animal wireless recording techniques that allowed us to record from several brains at the same time while bats were free to behave as they naturally would while clustered in the wild. Thus, we could monitor the neural activity at the levels of individual neurons from several group members as they freely engage in social-vocal interactions.

Interestingly, we found that individual neurons in the cortex do not respond to specific acoustic features of social calls. However, single neuron activity distinguishes between making and hearing calls, creating a distinct representation of self and others. More strikingly, individual neuron activity could be used to distinguish the identity of individual group members above and beyond the distinctive acoustic features of their calls. This hints that these neurons integrate information from multiple sensory modalities and / or from contextual information to create a representation of an individual identity of other group members. 

In addition, recording from several animals at the same time allowed us to look at neural activity across the brains of group members. Here we found that the high frequency power of the local field potential shows an increase in the correlation between individuals during communication. This was true for listening and calling pairs, as well as between listening pairs. However, this was not the case when we played the recordings of the same social vocalizations to the bats, indicating that it is not just a shared vocal input that creates this synchronization but the social context of the call that is important. In addition, the level of correlation between pairs was not uniform, with some bat pairs having a higher level of correlation compared to others during calls, again suggesting that individuality was key. This pattern was stable across weeks, possibly reflecting stable social relationships within the group. This view was supported by additional experiments demonstrating that the social context was key to these neural findings. Specifically, when bats vocalized for reward, the activity within and across brains remapped completely. The same Individual neurons were no longer representing calls, with some neurons moving towards representing the reward instead. Even more so, the synchronization between bats was abolished during calls occurring outside the natural group social context. This finding strongly suggests that the activity patterns we find relate to the social context of communication. 

Finally, we asked if these activity patterns are affected by social preferences of individual group members. To test this, we preformed experiments in a larger enclosure that allowed the bats to move further away from other bats thus revealing their social-spatial preferences. We found that while all bats tend to spend most of their time within the group cluster, a minority of bats spend a significant portion of their time away from the group. We then asked if these bats elicit different neural responses when communicating within the group (all communication events were within the group setting). To our surprise, we find that both single neuron identity decoding, and inter-brain synchrony were significantly lower in the group when less social bats were communicating. This could indicate that less social bats are perceived differently in the mind of other group members, or that they are less effective at communicating, perhaps leading to their higher levels of isolation. 

Thus, by utilizing wireless multi-animal recordings in feely behaving bats in the group setting we found a dedicated neural repertoire for group social communication. These findings open a slew of questions that relate to elucidating how the cortex is able to integrate the required information to produce these intricate social representations and also may help identify when and how these neural representations fail, perhaps contributing to social deficits in effected individuals.         

HFSP award information

Long-Term Fellowship (LT000627/2021-L): Neuronal mechanisms underlying group social interactions in bats 

Fellow: Boaz Styr
Nationality: Israel/Poland
Host institution: University of California, Berkeley, USA
Host supervisor: Michael Yartsev

Reference

Cortical representation of group social communication in bats
Maimon C. Rose, Boaz Styr, Tobias A. Schmid, Julie E. Elie, Michael M. Yartsev 
SCIENCE, 22 Oct 2021, Vol 374, Issue 6566, DOI: 10.1126/science.aba9584

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Reference

Cortical representation of group social communication in bats
Maimon C. Rose, Boaz Styr, Tobias A. Schmid, Julie E. Elie, Michael M. Yartsev 
SCIENCE, 22 Oct 2021, Vol 374, Issue 6566, DOI: 10.1126/science.aba9584