Neural circuit tuning fly visual neurons to motion of small objects. II. Input organization of inhibitory circuit elements revealed by electrophysiological and optical recording techniques.

1. The FD1-cell in the visual system of the fly is an identified visual interneuron that is specifically tuned to motion of small objects. In the companion paper it was shown that this response property is mediated by one of the two CH-cells, the VCH-cell, that inhibits the FD1-cell by GABAergic synapses. Here the input organization of the two CH-cells is analyzed by both electrophysiological and optical recording techniques. 2. Both CH-cells are excited by front-to-back motion in the ipsilateral and by back-to-front motion in the contralateral visual field. They respond maximally to binocular rotatory motion about the vertical axis of the animal. The latter response is only slightly less than the sum of the corresponding monocular response components. The relative contribution of the ipsi-and contralateral eye to the binocular response varies considerably between flies. In extreme cases it is dominated by either the ipsi- or the contralateral eye. The two CH-cells are not equally sensitive along the vertical axis of the eye. The DCH-cell has its sensitivity maximum in the dorsal part, the VCH-cell in the ventral part of the visual field. 3. The CH-cells have two arborizations, a large one in the posterior part of the third visual neuropil, the lobula plate, and a smaller one in the ipsilateral ventrolateral brain. With the calcium-sensitive dye fura-2 as an activity marker, it is analyzed which of these branches of the CH-cells receive the ipsi- and contralateral motion input, respectively. During motion in the preferred direction within the ipsilateral visual field, calcium accumulates only in the CH-cells' main arborization in the lobula plate but not in their branches in the ventrolateral brain, indicating that the arborization in the lobula plate is postsynaptic to the ipsilateral input. In contrast, contralateral motion in the preferred direction leads to calcium accumulation in both arborizations, suggesting that both are postsynaptic to contralateral input elements. During preferred direction motion in the upper or lower part of the ipsilateral visual field, calcium accumulates in only dorsal or ventral branches of the CH-cells' arborization in the lobula plate, respectively, revealing that their ipsilateral motion input is organized retinotopically. Because this arborization, most likely, is also the main output terminal of the CH-cells, it is both pre- and postsynaptic. This specific neuronal design is discussed with respect to its consequences for the mechanism of tuning the FD1-cell to motion of small objects.