Mechanisms of punctuated vision in fly flight

Abstract

To guide locomotion, animals control their gaze via movements of their eyes, head, and/or body, but how the nervous system controls gaze during complex motor tasks remains elusive. Notably, eye movements are constrained by anatomical limits, which requires resetting eye position. By studying tethered, flying flies (Drosophila) in a virtual reality flight simulator, we show that ballistic head movements (saccades) reset eye position, are stereotyped and leverage elastic recoil of the neck joint, enabling mechanically assisted redirection of gaze. Head reset saccades were of proprioceptive origin and interrupted smooth movements for as little as 50 ms, enabling punctuated, near-continuous gaze stabilization. Wing saccades were modulated by head orientation, establishing a causal link between neck signals and execution of body saccades. Furthermore, we demonstrate that head movements are gated by behavioral state. We propose a control architecture for biological and bio-inspired active vision systems with limits in sensor range of motion.