Intrinsic properties of biological motion detectors prevent the optomotor control system from getting unstable

Abstract

Compensatory eye, head or body movements are essential to stabilize the gaze or the path of locomotion. Because such compensatory responses usually lag the sensory input by a time delay, the underlying control system is prone to instability, at least if it operates with a high gain in order to compensate disturbances efficiently. In behavioural experiments it could be shown that the optomotor system of the fly does not get unstable even when its overall gain is so high that, on average, imposed disturbances are compensated to a large extent. Fluctuations of the animal’s torque signal do not build up. Rather they are accompanied by only small-amplitude jittery retinal image displacements that rarely slip over more than a few neighbouring photoreceptors. Combined electrophysiological experiments on a pair of neurons in the fly’s optomotor pathway and model simulations of the optomotor control system suggest that this relative stability of the optomotor system is the consequence of the specific velocity dependence of biological movement detectors. The response of the movement detectors first increases with increasing velocity, reaches a maximum and then decreases again. As a consequence, large-amplitude fluctuations in pattern velocity, as are generated when the optomotor system tends to get unstable, are transmitted with a small gain leading to only relatively small torque fluctuations and, thus, small-amplitude image displacements.