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 ipsiand contralateral eye to the binocular response varies considerably between flies. In extreme cases it is dominated by either the ipsior 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 ipsiand 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 preand 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. J~LJKNALOF NEIJKOPHYSIOLOGY Vol. 69. No. 2. February 1993. it1 l;.S.,A. 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 MARTIN EGELHAAF, ALEXANDER BORST, ANNE-KATHRIN WARZECHA, SUSANNA FLECKS, AND ANKE WILDEMANN Mux-Planck-lnstitut fur hiologische Kyhernetik, W7400 Tiibingen, Germany . SUMMARY AND CONCLUSIONS I. The FDl -cell in the visual system of the f ly 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 FDl-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 arc 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 ipsiand contralateral eye to the binocular response varies considerably between flies. In extreme cases it is dominated by either the ipsior 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 furaas an activity marker, it is analyzed which of these branches of the CH-cells receive the ipsiand contralateral motion input, respectively. During motion in the preferred direction within the ipsilateral visual held, calcium accumulates only in the 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 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 preand postsynaptic. This specific neuronal design is discussed with respect to its consequences for the mechanism of tuning the FD l-cell to motion of small objects.