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Visuo-olfactory sensory fusion for flight behavior in flies
Mark Frye, Michael Dickinson

Over the past year I have used the support of this grant to study the neurobiological basis of multisensory flight control in flies. I have specifically focused on vision and olfaction and how feedback from these sensory modalities is integrated to coordinate complex spatiotemporal dynamics of search behaviors. Using a state-of-the-art stereo video system, I tracked freely flying flies within different sensory landscapes and found that visual expansion cues generated as flies approach vertical edges is required for odor localization (Fig. 5A). Using a 'virtual reality' tethered flight simulator, I examined the fine scale motor responses to visual expansion, odor, and both presented simultaneously. Our results show that during flight sensorimotor responses to odor are linearly superimposed upon visual responses (Fig. 5B). This is a remarkable finding because it suggests that – from an engineering perspective - the underlying neural processing for tracking multiple sensory cues is relatively simple. A parallel sensory-to-motor control architecture may be an evolutionary adaptation that imparts both the extraordinary flexibility and robustness exhibited by flies in diverse sensory landscapes. These results have culminated in one publication, presentations at two international meetings, and two more manuscripts to be submitted for publication this month.

Our recent results have shown that during odor search, Drosophila more closely approach visual features near an invisible odor source. Computer simulations based on free flight statistics showed that this vision-odor interaction is sufficient to enable flies to localize the odor. Quantitative analyses of animals' responses to different visual patterns revealed that the motion of vertical edges is the salient visual cue that interacts with olfactory feedback (Fig. 5A).

I further examined the fine scale of visuo-olfactory reflexes using a flight simulator in which I could manipulate a fly's visual and olfactory environment. Flies modulate wingbeat frequency and amplitude in response to visual and olfactory stimuli. Responses to both cues presented simultaneously represent the linear superposition of responses to stimuli presented in isolation for the onset and duration of odor delivery (Fig. 5B). This suggests that odor does not alter the time course or magnitude of visual reflexes. Visual feedback does, however, alter the time course of odor-off responses. Based on the physiology of the flight motor system and recent free-flight analyses, I have posited a model to account for multisensory integration for flight control, which suggests that visual and olfactory signals are selectively targeted to separate groups of flight muscles. A simple parallel hierarchy could produce complex flight maneuvers while preserving the sensitivity of each modality.

I have also examined how complex patterns of optic flow affect visual stabilization reflexes in flies. I found that flies are more sensitive to patterns of visual translation than patterns of rotation. Until now, the classic view of flight control had been founded on a linear model for the stabilization of image rotation. Our new findings suggest an alternate model that takes into account the complex patterns of optic flow experienced by animals in natural sensory landscapes.


 


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