Performance of fly visual interneurons during object fixation

Neurons involved in the processing of optic flow are usually analyzed using stimuli designed by the experimenter. However, in real life optic flow depends on locomotive behavior. We characterized the performance of motion-sensitive neurons in the visual system of the fly using optic flow as occurring in behavioral situations during object fixation. Optic flow generated by tethered flying flies in a flight simulator was subsequently replayed while recording the responses of two cell types in the fly's motion pathway presumably involved in the detection of objects and of deviations from a straight flight course, respectively. FD1b cells, which are representatives of the so-called figure-detection cells, responded very specifically to object motion. Although object selectivity of these cells is attributable to inhibition during large-field motion, the influence of background motion during object fixation was almost negligible. In contrast, the cells of the so-called horizontal system (HS cells) are most sensitive to background motion, as elicited during deviations of the animal from its course. During object fixation, the responses of HS cells depended on both object and background motion. The simulated distance of the background to the fly did not have a strong influence on the responses of either cell type. The specificity for detecting deviations from a straight course is enhanced by subtraction of the signals of HS cells in both halves of the brain. In contrast, the FD1b cells in the two halves of the brain need to interact in a nonlinear way to ensure efficient detection of objects.