Active vision shapes and coordinates flight motor responses in flies

Abstract

Animals use active sensing to respond to sensory inputs and guide future motor decisions. In flight, flies generate a pattern of head and body movements to stabilize gaze. How the brain relays visual information to control head and body movements and how active head movements influence downstream motor control remains elusive. Using a control theoretic framework, we studied the optomotor gaze stabilization reflex in tethered flight and quantified how head movements stabilize visual motion and shape wing steering efforts in fruit flies (Drosophila). By shaping visual inputs, head movements increased the gain of wing steering responses and coordination between stimulus and wings, pointing to a tight coupling between head and wing movements. Head movements followed the visual stimulus in as little as 10 ms-a delay similar to the human vestibulo-ocular reflex-whereas wing steering responses lagged by more than 40 ms. This timing difference suggests a temporal order in the flow of visual information such that the head filters visual information eliciting downstream wing steering responses. Head fixation significantly decreased the mechanical power generated by the flight motor by reducing wingbeat frequency and overall thrust. By simulating an elementary motion detector array, we show that head movements shift the effective visual input dynamic range onto the sensitivity optimum of the motion vision pathway. Taken together, our results reveal a transformative influence of active vision on flight motor responses in flies. Our work provides a framework for understanding how to coordinate moving sensors on a moving body.