Muscles that move the retina augment compound-eye vision in Drosophila

The majority of animals have compound eyes, with tens to thousands of lenses attached rigidly to the exoskeleton. A natural assumption is that all these species must resort to moving either their head or body to actively change their visual input. However, classic anatomy has revealed that flies have muscles poised to move their retinas under the stable lenses of each compound eye(1–3). Here we show that Drosophila use their retinal muscles to both smoothly track visual motion, which helps to stabilize the retinal image, and also to perform small saccades when viewing a stationary scene. We show that when the retina moves, visual receptive fields shift accordingly and that even the smallest retinal saccades activate visual neurons. Using a new head-fixed behavioral paradigm we find that Drosophila perform binocular, vergence movements of their retinas—which could enhance depth perception—when crossing gaps and impairing retinal-motor-neuron physiology alters gap-crossing trajectories during free behavior. That flies evolved an ability to actuate their retinas argues that moving the eye independently of the head is broadly paramount for animals. The similarities of smooth and saccadic movements of the Drosophila retina and the vertebrate eye highlights a notable example of convergent evolution.