Abstract

Visual identification of small moving targets is a challenge for all moving animals. Their own motion generates displacement of the visual surroundings, inducing wide-field optic flow across the retina. Wide-field optic flow is used to sense perturbations in the flight course. Both ego-motion and corrective optomotor responses confound any attempt to track a salient target moving independently of the visual surroundings. 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. 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. 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. 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. 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.

Highlights

  • Animals in motion generate large amounts of optic flow

  • Head movements are required for figure tracking against wide-field motion in closed-loop conditions We first measured the fly’s ability to actively track a moving randomly textured figure set against a randomly textured ground with their heads free to move (Fig. 1A, top row), and with their heads fixed in place with a drop of glue (Fig. 1A, bottom row)

  • When the figure was moving on a stationary ground, both groups of flies were able to robustly stabilize the figure in the frontal field of view, which results in a distinct peak in the probability density function of the figure’s position at 0 deg azimuth (Fig. 1A, left)

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Summary

Introduction

Animals in motion generate large amounts of optic flow. 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). In an analogous response, flying and walking insects produce optomotor adjustments of their wing kinematics to rotate their entire body and compensate for retinal slip

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