Date of Award
Doctor of Philosophy (PhD)
The diversity of behaviors exhibited by animals is astounding. Even within a species, members constantly select between a myriad of ways to interact with their environment, ranging from foraging to fighting. Yet, why an individual behaves as it does in each moment of time typically remains nebulous to us as observers. In this thesis, I explore the possibility that these seemingly idiosyncratic behavioral decisions can be understood by accessing the hidden internal motivations that spur an animal to do one thing in lieu of another. By leveraging the compact brain architecture and rich social behaviors of the fruit fly Drosophila melanogaster, I detail how internal drives are encoded in specific neural circuits, and how they pattern an animal’s behavior on a moment-tomoment basis by tuning both perception and action selection. In Drosophila, male flies perform a lengthy and elaborate courtship ritual that typically commences after they sample the pheromones of a suitable mate. The initiation of courtship represents a striking switch in a male’s behavior, as he transitions from being apathetic or “blind” to a female to vigorously tracking her for minutes at a time while singing a species-specific song. In chapters 2-4, I describe how the link between perception and action is dynamically reconfigured in the male brain at the onset of courtship to convert a female from an indifferent visual object to a target of desire. These studies were largely enabled by a preparation in which tethered flies can interact with a fly-sized visual target in virtual reality, which has allowed me to coordinately examine social behaviors and their underlying neural substrate for the first time. In Chapter 5, I explore how the behavioral flexibility afforded by the neural mechanisms described in the preceding chapters is employed in the context of the natural ecology of Drosophila. In the wild, flies meet and mate on fermenting fruits where a diversity of individuals congregate. Reproductive success in this complex social environment requires that a male fly not only doggedly pursues his mate of choice, but that he also effectively fights off rival males vying for the same female. Thus, a male’s sexual arousal must be balanced with competing drives to appropriately pattern social interactions in these naturalistic contexts. I will show that when a male transiently senses a cue emitted by male competitors, he switches from courting a visual target to exhibiting aggression towards it. These rapid behavioral transitions are mediated by a small population of higher-order neurons that function to regulate the expression of this aggression rather than courtship. Based on these results, I propose that the neural pathways mediating social interactions in the fly thus function like a switchboard, allowing incoming visual information to be flexibly rerouted to different motor pathways depending on a male’s motivational state and immediate sensory context to pattern his ongoing behavior. This provides a conserved logic for how the incredible diversity of behaviors expressed across the lifetime of an animal could be achieved, and suggests that we can account for much of the idiosyncrasies of animal behavior by examining ongoing transitions between competing needs and drives.
Sten, Tom Anton Hindmarsh, "The Internal Orchestration of a Courtship Ritual in Drosophila" (2023). Student Theses and Dissertations. 742.
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