Background

New method

Results

Comparison with existing methods

Conclusions

Many species negotiate complex spatial environments alongside other individuals and displaythe capacity to recall rewarding and costly locations. Prodigious navigators like the Egyptian fruit bats forage for food in convoluted aerial spaces and must account for the choices of other flying conspecifics to reach reward locations. We can simulate this challenging feat in the lab environment while using high-speed positional tracking and neural recording methods to investigate how bats solve this high-dimensional multi-agent foraging problem. However, in the lab the multi-agent foraging problem has a latent extra player: the human experimenter. While most studies involving a spatial reward task ignore the presence of the human in reporting and controls, we sought to explicitly include the experimenter in the task paradigm to test whether there is an appreciable effect of human presence on ongoing neural signal.

The first section of this thesis explores the neural representation of the human experimenterduring a multi-agent foraging task. We find that a substantial amount of variance in the code for allocentric spatial representation can be accounted for simply by controlling for the identity of the human the bat lands on. This study shows, for the first time, that non-conspecifics are encoded in the canonical place cell code for spatial position. On a practical level, these findings serve as a cautionary tale to encourage future studies to limit the uncontrolled effects of human presence and intervention in behavioral neuroscience tasks.

The second section of this thesis strips down the complex foraging problem to its simplest formto study the stability of the neural code that supports flight in a familiar foraging environment. We find that, across days, the code for flight is largely stable and apparent variance may be accounted for simply by behavioral drift, not changes in the underlying neural code.

The thesis concludes with caveats of the current research, possibilities for future investigation,and avenues for combining modeling work with cross-species representation in the environment.

Understanding how neural circuits control complex social and spatial behaviors in humans requires a tractable mammalian model system that allows one to probe both the appropriate behavior and its underlying neural activity. Egyptian fruit bats (Rousettus aegyptiacus) are an attractive model for studying the motor control of vocal communication and navigation. To thrive within hierarchical social structures in dark cave environments, bats evolved specialized auditory and vocal production systems to both echolocate and communicate with one another. However, to date, the detailed neural computations that support this behavior in mammals are unknown. Furthermore, in the wild, bats fly highly reproducible trajectories from their home cave to foraging sites over 20km round trip nightly. It is unclear whether the neural representation of these flight paths remains stable across days when a stable behavior is performed. In this thesis, I describe my efforts to study the behavior, anatomy, and neurophysiology of vocal communication and spatial navigation in a novel model organism.

In Chapter 1, I provide and introduction to theories of vocal learning, mammalian motor control of vocal production, and social communication. Furthermore, I provide a focused review of the hippocampal representation of place and current theories of how this representation changes across days. In Chapter 2, I present my efforts to design a behavioral task that operantly trained the bats to produce vocalizations for reward. Additionally, I present anatomical tracing data that identified the motor cortical site of laryngeal control and supports the theory of vocal learning in bats. Finally, I discuss collaborations to probe the underlying electrophysiology in this motor region during the vocal production task. In Chapter 3, I present my work developing a wireless miniature fluorescent microscope and its use to study the longitudinal stability of spatial coding in freely flying bats performing a self-paced navigation task. This work is presented as a manuscript (currently under review) with my co-author Dr. William Liberti.

Social interactions often occur in group settings and are mediated by communication signals that are exchanged between individuals, frequently utilizing vocalizations. The neural representation of group social communication remains largely unexplored. Here, 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 others, as well as among specific individuals. Coordinated neural activity among group members exhibited stable bidirectional inter-brain correlation patterns specific to spontaneous communicative interactions. Tracking social and spatial arrangements within a group revealed a relationship between social preferences and intra- and inter-brain activity patterns. We also present preliminary results relating to the neural correlates of social-vocal interactions in juvenile bats. Combined, these findings reveal a dedicated neural repertoire for group social communication within and across the brains of freely communicating groups of bats.