The role of horizontal system cells in optomotor responses in Drosophila melanogaster

When confronted with a large-field stimulus rotating around the vertical body axis, flies display a following behaviour of the head and steer in the direction of motion. As neural control elements for this so-called 'optomotor response', the large tangential horizontal cells (HS-cells) of the lobula plate have been the prime candidates for long. When HS-cells are surgically damaged or genetically removed, flies display reduced optomotor responses. To provide a better understanding of the role of HS-cells in the control of optomotor behaviour three approaches were taken. First, experiments were designed to investigate which of the HS-cells could be participating in head yaw movements in fixed flies and yaw turning behaviour during tethered flight. Horizontal motion at different elevations was presented to the flies. Comparison of the optomotor responses with HS-cell receptive fields suggests that HSN and HSE participate in head yaw movements whereas all three HS-cells are used to control yaw turning behaviour during flight. Second, to test whether HS-cells are sufficient to elicit yaw optomotor responses, a bi-stable Channelrhodopsin-2 variant 'ChR2 (C128S)' was expressed in HS-cells using the Gal4 / UAS-system. Combining a blue light stimulus with ChR2(C128S) allowed to activate HS-cells without presenting a visual stimulus to the eye of the fly. These experiments revealed that blue light was sufficient to evoke robust head yaw movement in fixed flies as well as turning behaviour in tethered flying flies, thus, mimicking front-to-back visual stimulation on the stimulated side. Third, the role of the receptive field layouts of HS-cells for optomotor responses was studied. Flies with a gain-of-function of a single Dscam1 isoform in all HS-cells (Dscam gain-of-function (D(GOF)) flies) were tested. Compared with HS-cells of control flies, HS-cells of D(GOF) flies show reduced sensitivity to horizontal motion in the frontal and enhanced sensitivity to motion in the lateral part of visual space. The optomotor response of tethered flying flies were analyzed. Compared with control flies, D(GOF) flies responded significantly weaker to visual stimuli extending over the entire azimuth extension of HS-cell receptive fields. Stimulating flies with additional motion in the rear part of visual space significantly reduced optomotor responses of control flies, whereas (GOF) flies responded to both visual stimuli with about equal strength. Although D(GOF) HS-cells had dramatically reduced sensitivity to motion in the frontal part of visual space, D(GOF) flies responded robustly to motion in this region of visual space. D(GOF) and control flies also showed differences in head yaw movements. These behavioural differences did not correlate with the difference in the receptive fields of D(GOF) and control HS-cells. The experiments indicate that HS-cells are sufficient to trigger yaw turns of the head and whole body. All three HS-cells control body turns during flight and head yaw turns are controlled by HSN- and HSE-cells. The layout of HS-cell receptive fields, however, does not correlate 1 : 1 with optomotor responses. During flight, flies rely additionally on cells sensitive in the frontal part of visual space. Furthermore, the layout of the HS-cell receptive fields is important for incorporating motion information in the rear part of visual space to the optomotor responses.