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On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster

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Summary

Yaw torque fluctuations ofDrosophila in stationary flight at the torque meter in many cases represent meaningful behavior patterns (e.g., Figs. 4, 9a). In the closed loop situation for rotations around the fly's vertical axisDrosophila stabilizes any panorama by adjusting its “optomotor balance” (e.g., Figs. 2, 3, 8, 11) — a presumably integrative directionally movement sensitive flight control mechanism.

In this state of “harmony” with the environmentDrosophila often performs active turns by means of body-saccades (Fig. 2). In this study these are recorded as “torque spikes” — an elementary motor pattern of typical size and time course (Fig. 3). Their polarity and frequency are dependent upon visual stimulation (Figs. 4, 5, 6).

During a torque spike the fly does not respond to the visual stimulation caused by the relative displacement of the environment (Fig. 13); an artificial displacement in the opposite direction, however, causes a fast vigorous turning response. This is attributed to a directionally selectiveefference copy of the torque spike motor pattern which suppresses the reafferent visual input (Fig. 13a-f). The efference copy also relieves the visual system from certain inhibitory interactions which, in larger flies, have been shown to provide “figure-ground” discrimination (Fig. 13g-l). In addition the asymmetry in the fly's response to progressive and to regressive movement of small patterns is eliminated by the efference copy. Such information processing steps may be of minor importance during body-saccades.

Optomotor balance inDrosophila is the basis of oriented flight. In closed loop experiments with one vertical black stripe the fly spends only part of its time keeping the stripe in its direction of flight (fixation). More often it stabilizes the stripe in other positions (non-fixation) (Fig. 8). Torque responses to the position of objects inDrosophila appear to be centrally controlled. Various situations in which the fly favors fixation (anti-fixation) or non-fixation are described.

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We wish to thank J. Blondeau, K.-F. Fischbach, K.G. Götz, M.F. Land, E. Linsenmair, T. Poggio and W. Reichardt for stimulating discussions and helpful comments on a preliminary version of this paper. We are also grateful to Mrs. K. Schulze for typing the manuscript. The Max-Planck-Institut für biologische Kybernetik, Tübingen, provided parts of the equipment. This work was supported by a Deutsche Forschungsgemeinschaft grant to M.H.

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Heisenberg, M., Wolf, R. On the fine structure of yaw torque in visual flight orientation ofDrosophila melanogaster . J. Comp. Physiol. 130, 113–130 (1979). https://doi.org/10.1007/BF00611046

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