On the neuronal basis of figure-ground discrimination by relative motion in the visual system of the fly

Abstract

A fly can discriminate an object ("figure") from its background on the basis of motion information alone. This information processing task has been analysed, so far, mainly in behavioural studies but also in electrophysiological experiments (Reichardt et al., 1983). The present study represents a further attempt to bridge the gap between the behavioural and the neuronal level. It is based on behavioural and electrophysiological experiments as well as on computer simulations. The characteristic properties of figureground discrimination behaviour impose specific constraints on the spatial integration properties of the output cells of the underlying neuronal network, the heterolateral interactions in their input circuitry, as well as on the range of variability of their response. These constraints are derived partly from previous behavioural studies (Reichardt et al., 1983), partly, however, from behavioural response characteristics which have not been addressed explicitly so far. They are interpreted in terms of one of the alternative model circuits shown by Reichardt et al. (1983) to be sufficient to account for figure-ground discrimination. It will be demonstrated, however, that this can be done equally well by means of a further alternative model circuit. These constraints are used in the electrophysiological analysis for establishing visual interneurones as output elements of the neuronal network underlying figure-ground discrimination. In the behavioural experiments on figure-ground discrimination as well as on the optomotor course control the yaw torque generated by the tethered flying fly under visual stimulation was used as a measure for the strength and time course of the reaction. Therefore, it has initially been proposed that the three Horizontal Cells, which are regarded as the output elements of the neuronal network underlying the optomotor reaction (e.g. Hausen, 1981), might also control yaw torque generation in figure-ground discrimination (Reichardt et al., 1983). New behavioural data show, however, that the Horizontal Cells do not meet all the constraints imposed on the presumed output cells of the figure-ground discrimination network: (1) The Horizontal Cells are not sensitive enough to motion of small objects. (2) The heterolateral interactions within their input circuitry are not in accordance with the behavioural data (see also Reichardt et al., 1983). (3) The variability found in the time course of certain components of the yaw torque response to relative motion of figure and ground cannot be explained by their response characteristics. Hence, the Horizontal Cells cannot account for figure-ground discrimination on their own and additional output cells of the optic lobes with different functional properties are required to accomplish this task.