Characterizing odor motion detection in flies

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Many animals rely on their ability to navigate to the source of airborne odor plumes for survival. Studies dating back a century have shown that insects combine mechanosensory and olfactory cues to navigate, surging upwind when detecting odor but go crosswind or downwind when losing the signal. They also use bilateral information from their two antennae to turn toward higher odor concentrations. We recently discovered that in addition to wind direction and odor gradient, fruit flies detect the direction of motion of odors, independent of the wind. Using optogenetics to decouple odor signal from wind, we found that flies detect odor motion using the temporal correlations of the odor signal between their two antennae, suggesting similarities with motion detection in vision. Manipulating spatio-temporal correlations in virtual odor signals demonstrated that flies indeed exploit odor motion when navigating odor plumes. The finding that Drosophila melanogaster can ‘smell’ odor motion suggests a novel role for bilateral sensing in olfaction and raises the following questions for the field: 1) How is odor motion — a previously unappreciated olfactory directional cue — integrated with other directional cues to drive olfactory navigation? 2) What are the inputs to the odor motion detector and how does odor valence modulate behavioral response to odor motion? 3) What neural circuits and computations mediate odor motion detection and how do they compare to those that mediate visual motion detection? We will address these questions by combining optogenetic stimulation, neuron activity measurements, and neurogenetic silencing with the behavioral and computational framework we used to discover odor motion sensing. With this platform we can control, measure, and perturb real odor and virtual odor signals in closed- and open-loop, during olfactory navigation of freely walking flies. Drosophila is perfectly suited to pursue these goals because of 1) the current knowledge of the neural circuit of the olfactory periphery and increasingly of downstream olfactory centers, and the availability of a connectome; and (2) the ability to selectively measure and manipulate the activity of neural circuits involved in sensory processing and integration. The finding that flies use odor motion detection to enhance odor-guided navigation reveals important gaps in our understanding of olfactory navigation. The proposed research will close these gaps by characterizing how flies integrate odor motion with other cues to direct olfactory behavior, and by uncovering the neural circuits and computations that mediate odor motion detection. More broadly, these findings will advance our understanding of neuronal circuit computations by allowing us to compare circuits that compute motion across the modalities of olfaction and vision, which derive these signals from inputs with very different statistics and use them for different navigational purposes.