Oculomotor control in calliphorid flies: head movements during activation and inhibition of neck motor neurons corroborate neuroanatomical predictions.

In tethered flying flies, moving contrast gratings or small spots elicit head movements which are suited to track retinal images moving at velocities up to 3,000 degrees/sec (about 50 Hz contrast frequency for gratings of spatial wavelength 15 degrees). To investigate the neural basis of these movements we have combined videomicroscopy with electrophysiological stimulation and recording to demonstrate that excitation of prothoracic motor neurons projecting in the anterodorsal (ADN) and frontal nerves (FN), respectively, generates the yaw and roll head movements measured behaviorally. Electrical stimulation of the ADN produces head yaw. The visual stimuli which excite the two ADN motor neurons (ADN MNs) are horizontal motion of gratings or spots moving clockwise around the yaw axis in the case of the right ADN (counterclockwise for left ADN). Activity is inhibited by motion in the opposite direction. Spatial sensitivity varies in the yaw plane with a maximum between 0 degree and 40 degrees ipsilaterally, but both excitation and inhibition are elicited out to 80 degrees in the ipsilateral and contralateral fields. ADN MNs respond to contrast frequencies up to 15-20 Hz, with a peak around 2-4 Hz for grating motion in the excitatory or inhibitory directions. Electrical stimulation of the FN primarily elicits roll down to the ipsilateral side. The one FN MN consistently driven by visual stimulation is excited by downward motion and inhibited by upward motion at 80 degrees azimuth in the ipsilateral visual field. At -80 degrees contralateral, visual motion has the opposite effect: Upward is excitatory and downward is inhibitory. The FN MN is tuned to contrast frequencies in the same range as the ADN MNs, with peak sensitivity around 4 Hz. The functional organization of inputs to the ADN and FN is discussed with respect to identified visual interneurons and parallel pathways controlling motor output.