Hummingbirds use compensatory eye movements to stabilize both rotational and translational visual motion

To maintain stable vision, behaving animals make compensatory eye movements in response to image slip, a reflex known as the optokinetic response (OKR). Although OKR has been studied in several avian species, eye movements during flight are expected to be minimal. This is because vertebrates with laterally placed eyes typically show weak OKR to nasal-to-temporal motion (NT), which simulates typical forward locomotion, compared with temporal-to-nasal motion (TN), which simulates atypical backward locomotion. This OKR asymmetry is also reflected in the pretectum, wherein neurons sensitive to global visual motion also exhibit a TN bias. Hummingbirds, however, stabilize visual motion in all directions through whole-body movements and are unique among vertebrates in that they lack a pretectal bias. We therefore predicted that OKR in hummingbirds would be symmetrical. We measured OKR in restrained hummingbirds by presenting gratings drifting across a range of speeds. OKR in hummingbirds was asymmetrical, although the direction of asymmetry varied with stimulus speed. Hummingbirds moved their eyes largely independently of one another. Consistent with weak eye-to-eye coupling, hummingbirds also exhibited disjunctive OKR to visual motion simulating forward and backward translation. This unexpected oculomotor behaviour, previously unexplored in birds, suggests a potential role for compensatory eye movements during flight.