Synaptic organization of starburst amacrine cells in rabbit retina: Analysis of serial thin sections by electron microscopy and graphic reconstruction

Abstract

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 int he 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.(ABSTRACT TRUNCATED AT 400 WORDS)

AMPA receptors mediate acetylcholine release from starburst amacrine cells in the rabbit retina

“…Type b cells have perikarya displaced to the ganglion cell layer, processes ramifying in stratum 4 (S4) of the IPL and ON responses to light (Famiglietti, 1983;Tauchi and Masland, 1984;Vaney, 1984;Bloomfield and Miller, 1986). In rabbits, starburst amacrine cells are known to receive synaptic inputs from cone (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991).…”

“…Instead, amacrine cells with somata in the ganglion cell layer and labeled with DAPI were targeted, and either individual cells or 2-3 neighboring cells were injected intracellularly with Neurobiotin. The injected neurons were identified as starburst amacrine cells based on their characteristic morphology, and the proximal, intermediate, and distal dendritic zones were defined according to Famiglietti (1991). Both GluR4-IR and GluR2/3-IR puncta were localized on the dendrites of starburst cells and both types of AMPA receptor subunits appeared to have similar distributions along the dendrites.…”

“…Type b cells have perikarya displaced to the ganglion cell layer, processes ramifying in stratum 4 (S4) of the IPL and ON responses to light (Famiglietti, 1983;Tauchi and Masland, 1984;Vaney, 1984;Bloomfield and Miller, 1986). In rabbits, starburst amacrine cells are known to receive synaptic inputs from cone (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991).Starburst amacrine cells synthesize and release both γ-aminobutyric acid (GABA) and acetylcholine (ACh) when depolarized (Masland and Livingstone, 1976;Massey and Neal, 1979;O'Malley and Masland, 1989). ACh release from the rabbit retina increases at both light onset and light offset and is maximally stimulated by large stimuli at temporal frequencies of 1-4 Hz (Massey and Neal, 1979;Massey and Redburn, 1985;O'Malley and Masland, 1993).…”

“…bipolar cells and amacrine cells, including other starburst cells (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991).…”

“…ACh release from the rabbit retina increases at both light onset and light offset and is maximally stimulated by large stimuli at temporal frequencies of 1-4 Hz (Massey and Neal, 1979;Massey and Redburn, 1985;O'Malley and Masland, 1993). The majority of the synaptic output from the starburst cells is onto ganglion cell dendrites (Brandon, 1987;Millar and Morgan, 1987;Famiglietti, 1991). Starburst amacrine cells are known to provide a major synaptic input to directionally selective ganglion cells, but it is uncertain what role they play in establishing the selectivity of their responses (reviewed in Vaney and Taylor, 2002).…”