Evidence for one-way movement detection in the visual system of Drosophila.

Abstract

Optomotor control of course and altitude in the fruitfly, Drosophila melanogaster, requires dense networks of elementary movement detectors (EMD's) which cover most if not all of the visual field. The predominant types of EMD's in these networks represent interactions between neighbouring visual elements along the three main directions of the hexagonal array in the compound eye. -- Course control in the walking fly is achieved mainly by pairs of equivalent EMD's which occupy 2 o'clock and 4 o'clock positions with respect to the right eye (Buchner, 1976). Comparison of the turning response and the torque response in the present account confirms the particular properties of this network, and proves the presumed bidirectional sensitivity of its EMD's for the course control responses of legs and wings in the corresponding modes of locomotion. -- Altitude control during flight is achieved by a less homogeneous network of EMD's which modifies lift and thrust simultaneously by the appropriate control of the wing beat amplitudes. The predominant types of EMD's in the lateral eye regions occupy 12 o'clock and 2 o'clock positions with respect to the right eye (Buchner et al., 1978). The present evaluation of the optomotor responses of thrust and wing beat confirms the preferred orientation of these EMD's and discloses a pecularity of their internal structure. The movement detectors of this network lack the bidirectional sensitivity of the EMD's in the course control system. At least the fronto-lateral network of the altitude control system seems to consist mainly of pairs of equivalent unidirectional EMD's. The detectors in 12 o'clock position increase wing beat in response to movement of the visual surroundings from inferior to superior. The opposite effect is produced by the detectors in 2 o'clock position which respond to movement from anterior-superior to posterior-inferior. These properties qualify unidirectional EMD's as the functional units of the optomotor control system in the fruitfly. Pairs of unidirectional antagonists would be sufficient to establish the bidirectional sensitivity found in the movement detectors of the course control system.