Synaptic organization of complex ganglion cells in rabbit retina: type and arrangement of inputs to directionally selective and local-edge-detector cells.

The type and topographic distribution of synaptic inputs to a directionally selective (DS) rabbit retinal ganglion cell (GC) were examined and were compared with those received by two other complex GC types. The percentage of cone bipolar cell (BC) input, presumably an index of sustained responses and simple receptive field properties, is much higher than expected for complex GCs in reference to previous reports in other species: approximately 20% for the type 1 bistratified ON-OFF DS GC and for a multistratified GC, and approximately 40% for the small-tufted local-edge-detector GC. Consistent with a previous study (Famiglietti [1991] J. Comp. Neurol. 309:40-70), no ultrastructural evidence is found for inhibitory synapses from starburst amacrine cells to the ON-OFF DS GC. The density of inputs to the ON-OFF DS GC is high and rather evenly distributed over the dendritic tree. Clustering of inputs brings excitatory and inhibitory inputs into proximity, but the strict on-path condition of more proximal inhibitory inputs, favoring shunting inhibition, is not satisfied. Prominent BC input and its regional variation suggest that BCs play key roles in DS neural circuitry, both pre- and postsynaptic to the ON-OFF DS GC, according to a bilayer model (Famiglietti [1993] Invest. Ophthalmol. Vis. Sci. 34:S985). Asymmetry of inhibitory amacrine cell input may signify a region on the preferred side of the receptive field, the inhibition-free zone (Barlow and Levick [1965] J. Physiol. (Lond.) 178:477-504), supporting a role for postsynaptic integration in the DS mechanism. Prominent BC input to the local-edge-detector, often without accompanying amacrine cell input, indicates presynaptic integration in forming its trigger feature.