Summary

A computerized 360 degrees panorama allowed us to suppress most of the locomotion-induced visual feedback of a freely walking fly without neutralizing its mechanosensory system ('virtual open-loop' conditions). This novel paradigm achieves control over the fly's visual input by continuously evaluating its actual position and orientation. In experiments with natural visual feedback (closed-loop conditions), the optomotor turning induced by horizontal pattern motion in freely walking Drosophila melanogaster increased with the contrast and brightness of the stimulus. Conspicuously striped patterns were followed with variable speed but often without significant overall slippage. Using standard open-loop conditions in stationary walking flies and virtual open-loop or closed-loop conditions in freely walking flies, we compared horizontal turning induced by either horizontal or vertical motion of appropriately oriented rhombic figures. We found (i) that horizontal displacements and the horizontal-motion illusion induced by vertical displacements of the oblique edges of the rhombic figures elicited equivalent open-loop turning responses; (ii) that locomotion-induced visual feedback from the vertical edges of the rhombic figures in a stationary horizontal position diminished the closed-loop turning elicited by vertical displacements to only one-fifth of the response to horizontal displacements; and (iii) that virtual open-loop responses of mobile flies and open-loop responses of immobilized flies were equivalent in spite of delays of up to 0.1 s in the generation of the virtual stimulus. Horizontal compensatory turning upon vertical displacements of oblique edges is quantitatively consistent with the direction-selective summation of signals from an array of elementary motion detectors for the horizontal stimulus components within their narrow receptive fields. A compensation of the aperture-induced ambiguity can be excluded under these conditions. However, locomotion-induced visual feedback greatly diminished the horizontal-motion illusion in a freely walking fly. The illusion was used to assay the quality of open-loop simulation in the new paradigm.