SUMMARYIn most animals, the visual system plays a central role in locomotor guidance. Here, we examined the functional organization of visuomotor reflexes in the fruit fly, Drosophila, using an electronic flight simulator. Flies exhibit powerful avoidance responses to visual expansion centered laterally. The amplitude of these expansion responses is three times larger than those generated by image rotation. Avoidance of a laterally positioned focus of expansion emerges from an inversion of the optomotor response when motion is restricted to the rear visual hemisphere. Furthermore, motion restricted to rear quarter-fields elicits turning responses that are independent of the direction of image motion about the animal's yaw axis. The spatial heterogeneity of visuomotor responses explains a seemingly peculiar behavior in which flies robustly fixate the contracting pole of a translating flow field.

SUMMARY To study the visual cues that control steering behavior in the fruit fly Drosophila melanogaster, we reconstructed three-dimensional trajectories from images taken by stereo infrared video cameras during free flight within structured visual landscapes. Flies move through their environment using a series of straight flight segments separated by rapid turns, termed saccades, during which the fly alters course by approximately 90° in less than 100 ms. Altering the amount of background visual contrast caused significant changes in the fly’s translational velocity and saccade frequency. Between saccades, asymmetries in the estimates of optic flow induce gradual turns away from the side experiencing a greater motion stimulus, a behavior opposite to that predicted by a flight control model based upon optomotor equilibrium. To determine which features of visual motion trigger saccades, we reconstructed the visual environment from the fly’s perspective for each position in the flight trajectory. From these reconstructions, we modeled the fly’s estimation of optic flow on the basis of a two-dimensional array of Hassenstein–Reichardt elementary motion detectors and, through spatial summation, the large-field motion stimuli experienced by the fly during the course of its flight. Event-triggered averages of the large-field motion preceding each saccade suggest that image expansion is the signal that triggers each saccade. The asymmetry in output of the local motion detector array prior to each saccade influences the direction (left versus right) but not the magnitude of the rapid turn. Once initiated, visual feedback does not appear to influence saccade kinematics further. The total expansion experienced before a saccade was similar for flight within both uniform and visually textured backgrounds. In summary, our data suggest that complex behavioral patterns seen during free flight emerge from interactions between the flight control system and the visual environment.

SUMMARYFlies rely heavily on visual feedback for several aspects of flight control. As a fly approaches an object, the image projected across its retina expands, providing the fly with visual feedback that can be used either to trigger a collision-avoidance maneuver or a landing response. To determine how a fly makes the decision to land on or avoid a looming object, we measured the behaviors generated in response to an expanding image during tethered flight in a visual closed-loop flight arena. During these experiments, each fly varied its wing-stroke kinematics to actively control the azimuth position of a 15°×15° square within its visual field. Periodically, the square symmetrically expanded in both the horizontal and vertical directions. We measured changes in the fly's wing-stroke amplitude and frequency in response to the expanding square while optically tracking the position of its legs to monitor stereotyped landing responses. Although this stimulus could elicit both the landing responses and collision-avoidance reactions, separate pathways appear to mediate the two behaviors. For example, if the square is in the lateral portion of the fly's field of view at the onset of expansion, the fly increases stroke amplitude in one wing while decreasing amplitude in the other, indicative of a collision-avoidance maneuver. In contrast, frontal expansion elicits an increase in wing-beat frequency and leg extension,indicative of a landing response. To further characterize the sensitivity of these responses to expansion rate, we tested a range of expansion velocities from 100 to 10 000° s-1. Differences in the latency of both the collision-avoidance reactions and the landing responses with expansion rate supported the hypothesis that the two behaviors are mediated by separate pathways. To examine the effects of visual feedback on the magnitude and time course of the two behaviors, we presented the stimulus under open-loop conditions, such that the fly's response did not alter the position of the expanding square. From our results we suggest a model that takes into account the spatial sensitivities and temporal latencies of the collision-avoidance and landing responses, and is sufficient to schematically represent how the fly uses integration of motion information in deciding whether to turn or land when confronted with an expanding object.

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