The optomotor equilibrium of the Drosophila navigation system

Abstract

In his discussion of the optomotor behaviour Kalmus claimed in 1964 that the visual systems of insects continuously resolve horizontal displacements relative to the surroundings into rotatory and translatory components, each associated with optomotor feedback of particular quality and sign. The feedback is supposed to achieve, simultaneously, minimization of the rotatory movements and maximization of the translatory movements, a behaviour repeatedly observed with actively moving insects such as the fruitfly Drosophila melanogaster. The present approach takes into account that the output of movement detectors in the visual system of insects is necessarily equivocal with respect to the speed of the stimulus (e.g. zero output at both zero and infinite speed). Decomposition of the stimulus is not feasible under these conditions. It is obviously the composite stimulus to which the insects respond. Moreover, there is experimental evidence that optomotor feedback on the translatory movement is not necessarily a response-determining factor in insects. The optomotor behaviour of the walking fruitfly is sufficiently described by the sum of its rotatory responses to the composite stimuli on either side. A diagram representing the expected rotatory response of the walking fruitfly as a function of both the rotatory and the translatory stimulus component is used to derive the prevailing traits of the behaviour in resting, rotating and floating environments, respectively. Most conspicuous is the inversion of the course-control response in about one half of the possible states of stimulation. This effect gives rise to at least some of the apparently spontaneous turns of actively moving insects which have been ascribed by v. Holst and Mittelstaedt to efferent commands from higher centres of the brain, according to their principle of reafference. The present results merely disprove the necessity of these commands. Inversion of the response is also an inherent property of the course-control systems of the optomotorically active insects. The expected increase of these inversions with closer proximity of the visual environment is found by observation of walking fruitflies. The relation between the rotatory and translatory movements of the freely walking fly and its state of stimulation in a given environment is used to describe the expected behaviour in terms of the most probable transition of state. The approach is based on estimates of the power required by the fly in order to maintain a given state against the torque that is produced by its course-control system in response to the optomotor stimulation. The most probable transition of state is apparently determined by the tendency of the fly to decrease the power requirement by appropriate adaptation of its rotatory movement. The transition may come to an end in one of the states of minimum power requirement where the speed of the rotating fly is held in a stable optomotor equilibrium. © 1975 Springer-Verlag.