SYNAPTIC ORGANIZATION OF STARBURST AMACRINE CELLS IN RABBIT RETINA - ANALYSIS OF SERIAL THIN-SECTIONS BY ELECTRON-MICROSCOPY AND GRAPHIC RECONSTRUCTION

The synaptic organization of starburst amacrine cells was studied by electron microscopy of individual or overlapping pairs of Golgi-impregnated cells. Both type a and type b cells were analyzed, the former with normally placed somata and dendritic branching in sublamina a, and the latter with somata displaced to the ganglion cell layer and branching in sublamina b. Starburst amacrine cells were thin-sectioned horizontally, tangential to the retinal surface, and electron micrographs of each section in a series were taken en montage. Cell bodies and dendritic trees were reconstructed graphically from sets of photographic montages representing the serial sections. Synaptic inputs from cone bipolar cells and amacrine cells are distributed sparsely and irregularly all along the dendritic tree. Sites of termination include the synaptic boutons of starburst amacrine cells, which lie at the perimeter of the dendritic tree in the "distal dendritic zone." In central retina, bipolar cell input is associated with very small dendritic spines near the cell body in the "proximal dendritic zone." The proximal dendrites of type a and type b cells generally lie in planes or "strata" of the inner plexiform layer (IPL), near the margins of the IPL. The boutons and varicosities of starburst amacrine cells, distributed in the distal dendritic zone, lie in the "starburst substrata," which occupy a narrow middle region in each of the two sublaminae, a and b, in rabbit retina. As a consequence of differences in stratification, proximal and distal dendritic zones are potentially subject to different types of input. Type b starburst amacrines do not receive inputs from rod bipolar terminals, which lie mainly in the inner marginal zone of the IPL (stratum 5), but type a cells receive some input from the lobular presynaptic appendages of rod amacrine cells in sublamina a, at the border of strata 1 and 2. There is good correspondence between boutons or varicosities and synaptic outputs of starburst amacrine cells, but not all boutons gave ultrastructural evidence of presynaptic junctions. The boutons and varicosities may be both pre- and postsynaptic. They are postsynaptic to cone bipolar cell and amacrine cell terminals, and presynaptic primarily to ganglion cell dendrites. In two pairs of type b starburst amacrine cells with overlapping dendritic fields, close apposition of synaptic boutons was observed, raising the possibility of synaptic contact between them. The density of the Golgi-impregnation and other technical factors prevented definite resolution of this question. No unimpregnated profiles, obviously amacrine in origin, were found postsynaptic to the impregnated starburst boutons. Nevertheless, synapses were occasionally formed between unimpregnated boutons that resembled neighboring impregnated boutons of starburst amacrine cells. The synaptic outputs of starburst amacrine cells commonly occur in clusters, with some participation of other amacrine cell input (presumably including GABAergic and glycinergic input) and cone bipolar cell input. Through these clusters, arrayed in a flanking gantlet, run fascicles of two to four ganglion cell dendrites joined by puncta adherentia. The major portion of these ganglion cell dendrites is thought to belong to type 1 bistratified, or ON-OFF directionally selective ganglion cells, and in sublamina b, also to ON directionally selective ganglion cells. The ultrastructural evidence and the synaptic organization of starburst amacrine cells is considered together with histochemical and pharmacological evidence in regard to the role of starburst amacrine cells in the mechanism of directional selectivity. The evidence appears to favor the proposal, formerly advanced, that starburst amacrine cells potentiate the excitatory drive to directionally selective and other types of retinal ganglion cells.