Complementary feedback control enables effective gaze stabilization in animals

Abstract

Significance In visually active animals, eye, head, and body movements are coordinated to direct gaze. Given their distinct mechanics, how does the nervous system weight their contribution? By combining experiments in flying flies with control theory, we show that flies implement an elegant solution to this problem: the lower inertia head is recruited for higher-frequency visual tasks and is sensitive to motion acceleration, whereas the higher inertia body is recruited for lower-frequency visual tasks and is sensitive to motion velocity. This complementary division of labor within the nervous system exhibits two hallmarks of optimality: an increase in task performance accompanied with a decrease in mechanical energy expenditure. Our model recapitulates classic primate head-eye coordination responses, suggesting convergent mechanisms across phyla.