The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster

Abstract

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.