Multisensory integration for active mechanosensation in Drosophila flight

To support robust behaviors in highly variable environments, animals rely on active sampling of their sensory surroundings. Here, we use tethered, flying Drosophila melanogaster and a multisensory behavioral apparatus simulating forward flight to determine how visual and mechanosensory information are integrated and control active movements of an important multimodal sensory organ, the antennae. We found that flies perform active antennal movements in response to varying airflow, and that the direction of these movements changes depending on the visual environment. Next, we found that antennal movements are amplified in the presence of visual motion, but only when the fly was flying. Through mechanical and optogenetic manipulation of mechanosensory input, we found that mechanosensory feedback is vital to antennal positioning at flight onset. Additionally, we observed unexpected changes in wingbeat frequency when the antenna was mechanically stabilized, suggesting that multiple antennal mechanosensors contribute to flight regulation. Finally, we show that integration of mechanosensory and visual cues for controlling antennal motion follows in a “winner-takes-all” paradigm dependent on the stimulus frequency, mirroring visuo-mechanosensory guided behaviors in other species. Together, these results reveal novel behavioral gating of sensory information and expand our understanding of the efferent control of active sensing.