Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster

Abstract

Flies 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 degrees x 15 degrees 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 degrees 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.