Coordinating behavioral sequencing and sidedness

Most animals evolved with bilateral symmetry. Yet, many behaviors, from tying shoelaces to playing sports, require asymmetric motions and frequent transitions between the use of different sides of the body. Sidedness (whether the movement is produced on the right or left side of the body) therefore constitutes a critical aspect of the behavior, in addition to the sequence of actions that compose a behavior. We do not know how neural circuits coordinate these two aspects of behavior in any system. To solve this problem, we take advantage of a quantifiable, yet complex behavior produced by Drosophila melanogaster that involves both motor sequencing and sidedness. During courtship, male flies vibrate one wing at a time to produce a highly dynamic song that they pattern into sequences of distinct syllables in response to sensory cues from the female. Using novel behavioral methods, we show that males seamlessly switch between wings during the ongoing song, choosing the one closest to the female, without disruption or alteration of the song sequence. Moreover, we show that female location is highly predictive of male wing choice in their monocular zone (when the male fly sees the female with only one eye). Wing choices become stochastic in the binocular zone, when the position of the female becomes ambiguous. Additionally, we show that sensory information across modalities play different roles in mediating wing usage. Furthermore, using genetic manipulations, optogenetics, and patch-clamp electrophysiology, we explore the roles of individual neurons in wing choices and song patterning. Our ongoing study focuses on the computational rules and circuit mechanisms by which ongoing sensory information patterns song sequences and mediates wing choices simultaneously. Our work ultimately seeks to uncover general principles of neural circuit function that will inform how the nervous system implements behavioral flexibility in more complex systems.