In blowflies, both the body and the head are stabilized during straight flight, and are tightly coordinated during saccadic turns such that head turns occur slightly later and faster than body turns, thereby minimizing the duration of motion blur ( van Hateren and Schilstra, 1999). Previous studies of head movements in free-flying blowflies ( Schilstra and van Hateren, 1998) and tethered flying Drosophila ( Duistermars et al., 2012) showed that head movements are tightly coupled to wing steering kinematics during high-velocity body rotations: the head turns in the same direction as the thorax with a small delay and slightly faster kinematics. Similarly, they may show stabilizing responses by independently orienting their gaze by moving their heads (and therefore their eyes, as the eyes are fixed to the head). In an analogous response, flying and walking insects produce optomotor adjustments of their wing kinematics to rotate their entire body and similarly compensate for retinal slip ( Hassenstein and Reichardt, 1956 Götz and Wenking, 1973 Götz, 1975). In vertebrates, rotations of the eyes allow the animal to stabilize retinal slip ( Steinman and Collewijn, 1980 Miles, 1997). Throughout the animal kingdom, perturbations to optic flow induce an optokinetic reflex in which the animal will attempt to minimize the perceived slip of the retinal image by compensatory head, eye or body movements ( Paulus et al., 1984 Lappe et al., 1999). These results suggest that whereas figure tracking by wing kinematics is independent of head movements, head movements are important for stabilizing ground motion during active figure tracking.Īnimals in motion generate large amounts of optic flow. To our knowledge, this is the first demonstration that wing responses can be uncoupled from head responses and that the two follow distinct trajectories in the case of simultaneous figure and ground motion.
When a figure is moving relative to a moving ground, wing steering responses follow components of both the figure and ground trajectories, but head movements follow only the ground motion. We found that fixing the head in place impairs object fixation in the presence of ground motion, and that head movements are necessary for stabilizing wing steering responses to wide-field ground motion when a figure is present. What are the strategies that flying animals use to discriminate small-field figure motion from superimposed wide-field background motion? We examined how fruit flies adjust their gaze in response to a compound visual stimulus comprising a small moving figure against an independently moving wide-field ground, which they do by re-orienting their head or their flight trajectory. Both ego-motion and corrective optomotor responses confound any attempt to track a salient target moving independently of the visual surroundings. Wide-field optic flow is used to sense perturbations in the flight course.
Their own motion generates displacement of the visual surroundings, inducing wide-field optic flow across the retina. Visual identification of small moving targets is a challenge for all moving animals.