Visually Mediated Control of Flight in Drosophila: Not Lost in Translation

Flying insects exhibit stunning behavioral repertoires that are largely mediated by the visual control of flight. For this reason, presenting a controlled visual environment to tethered insects has been and continues to be a powerful tool for studying the sensory control of complex behaviors. The work presented in this dissertation concerns several robust behavioral responses exhibited by Drosophila that shed light on some of the challenges of visual navigation. To address questions of visual flight control in Drosophila, a modular display system has been designed and has proven to be a robust experimental instrument. The display system has enabled the wide variety of experimental paradigms presented in the thesis. Much is known about the responses of tethered Drosophila to rotational stimuli. However, the processing of the more complex patterns of motion that occur during translatory flight is largely unknown. Recent experimental results have demonstrated that Drosophila turn away from visual patterns of expansion. However, the avoidance of expansion is so vigorous, that flies robustly orient towards the focus of contraction of a translating flow field. Much of the effort documented in this thesis has sought to explain this paradox. The paradox has been largely resolved by several significant findings. When undergoing flight directed towards a prominent object, Drosophila will tolerate a level of expansion that would otherwise induce avoidance. The expansion-avoidance behavior is also critically dependent on the speed of image motion; in response to reduced speeds of expansion, Drosophila exhibit a centering response in which they steer towards the focus of expansion by balancing the image motion seen by both eyes. Taken together, these behaviors contribute to a model of Drosophila's visual flight control as emerging from multiple behavioral modules that operate concurrently. Simple computational models of Drosophila's visual system are used to demonstrate that the experimental results arrived at by doing psychophysics on tethered animals actually yield sensible navigation strategies. This final component of the thesis documents an effort to close the feedback loop around the experimenter, by using computational models of Drosophila behavior to constrain the design of future experiments.