Head movements quadruple the range of speeds encoded by the insect motion vision system in hawkmoths

Flying insects use compensatory head movements to stabilize gaze. Like other optokinetic responses, these movements can reduce image displacement, motion and misalignment, and simplify the optic flow field. Because gaze is imperfectly stabilized in insects, we hypothesized that compensatory head movements serve to extend the range of velocities of self-motion that the visual system encodes. We tested this by measuring head movements in hawkmoths Hyles lineata responding to full-field visual stimuli of differing oscillation amplitudes, oscillation frequencies and spatial frequencies. We used frequency-domain system identification techniques to characterize the head's roll response, and simulated how this would have affected the output of the motion vision system, modelled as a computational array of Reichardt detectors. The moths' head movements were modulated to allow encoding of both fast and slow self-motion, effectively quadrupling the working range of the visual system for flight control. By using its own output to drive compensatory head movements, the motion vision system thereby works as an adaptive sensor, which will be especially beneficial in nocturnal species with inherently slow vision. Studies of the ecology of motion vision must therefore consider the tuning of motion-sensitive interneurons in the context of the closed-loop systems in which they function.