Optomotor control of course and altitude in Drosophila melanogaster is correlated with distinct activities of at least three pairs of flight steering muscles.

Abstract

Flight control in the fruitfly Drosophila melanogaster is achieved by minute sets of muscles on either side of the thorax. Control responses of wings and muscles were elicited during fixed flight by moving a striped pattern in front of the eyes. For example, pattern motion from the lower right to the upper left signals to the test fly a rotatory course deviation to the right and simultaneously a translatory altitude displacement downwards. The counteracting response to the displacement of the retinal image is an increase in thrust and lift on the right, accomplished mainly by increasing the wingbeat amplitude (WBA) on that side. A comparison of such responses with the simultaneously recorded action potentials in the prominent basalar muscles M.b1 and M.b2 and axillary muscles M.I1 and M.III1 on either side suggests that three of these muscles act on the WBA more or less independently and contribute to the optomotor control of course and altitude. During flight, M.b1 is almost continuously active with a frequency equal to or slightly below 1 spike per wingbeat cycle. The spikes occur within a narrow phase interval of this cycle, normally at the beginning of the transition from upstroke to downstroke. However, the visual stimulus described above causes a substantial phase lead in M.b1 on the right; the spikes occur shortly before the end of the upstroke. Such phase shifts are accompanied by comparatively smooth 'tonic' responses of the WBA. The activities of M.b2 and M.I1 are normally very low. However, the stimulus described above activates M.b2 on the right in a phase interval approximately two-thirds into the upstroke and M.I1 on the left in a phase interval at the beginning of the downstroke. The spikes tend to occur in bursts. These bursts are correlated with WBA-increasing 'hitches' (rapid changes in amplitude) on the right and WBA-decreasing hitches on the left. As fast 'phasic' responses, the burst-induced hitches are likely to account for the course-controlling 'body saccades' observed during free flight. For unknown reasons, M.I1 is activated by pattern motion but cannot conceivably assist the other muscles in altitude control. Unlike its homologues in larger flies (Musca domestica, Calliphora erythrocephala), M.III1 does not participate in optomotor flight control. Its activation seems to support the termination of flight and wing retraction at rest. The essential properties of the three pairs of muscles M.b1, M.b2 and M.I1 resemble those found in larger flies; the muscles are controlled by motion detectors with muscle-specific 'preferred directions' in the hexagonal array of retinal elements. Optomotor control of the three pairs of muscles in Drosophila melanogaster could explain most, but not all, of the WBA responses recorded so far.