Receptive field properties of rod-driven horizontal cells in the skate retina.

Abstract

The large receptive fields of retinal horizontal cells result primarily from extensive intercellular coupling via gap (electrical) junctions; thus, the extent of the receptive field provides an index of the degree to which the cells are electrically coupled. For rod-driven horizontal cells in the dark-adapted skate retina, a space constant of 1.18 -+ 0.15 mm (SD) was obtained from measurements with a moving slit stimulus, and a comparable value (1.43 -+ 0.55 mm) was obtained with variation in spot diameter. These values, and the extensive spread of a fluorescent dye (Lucifer Yellow) from the site of injection to neighboring cells, indicate that the horizontal cells of the all-rod retina of skate are well coupled electrically. Neither the receptive field properties nor the gap-junctional features of skate horizontal cells were influenced by the adaptive state of the retina: (a) the receptive field organization was unaffected by light adaptation, (b) similar dye coupling was seen in both dark-and light-adapted retinae, and (c) no significant differences were found in the gap-junctional particle densities measured in darkand light-adapted retinas, i.e., 3,184 -286/p.m ~ (n = 8) and 3,073 -+ 494/1~m 2 (n = 11), respectively. Moreover, the receptive fields of skate horizontal cells were not altered by either dopamine, glycine, GABA, or the GABAA receptor antagonists bicuculline and picrotoxin. We conclude that the rod-driven horizontal cells of the skate retina are tightly coupled to one another, and that the coupling is not affected by photic and pharmacological conditions that are known to modulate intercellular coupling between cone-driven horizontal cells in other species.

Modulation of perch connexin35 hemi‐channels by cyclic AMP requires a protein kinase A phosphorylation site

“…The pharmacological properties of electrical synapses between retinal neurons can differ significantly, depending on the species studied. For example, gap junction channels between rod‐driven horizontal cells of the skate are distinct from those of cone‐driven horizontal cells and AII amacrine cells in other species with respect to their sensitivity to dopamine and cAMP analogs (Qian and Ripps, 1992). Although the exact cellular localization of skate Cx35 has not yet been determined, its close sequence homology to perch Cx35 (O'Brien et al, 1998) prompted us to compare the susceptibility of skate hemi‐channels to 8‐Br‐cAMP modulation.…”

“…A major physiological difference exists between these two fish, however, as skate has only one type of photoreceptors and is a pure rod retina. Although there have been no comparative reports of the action of dopamine and cAMP‐elevating drugs on gap junctions between AII amacrine cells in the two species, previous studies have demonstrated that electrical synapses between rod‐driven horizontal cells of the skate retina are not sensitive to treatment with dopamine and cAMP analogs (Qian and Ripps, 1992, Qian et al, 1993), thus setting them apart from the cone‐driven horizontal cells of other species that are uncoupled by the same pharmacologic treatments (Piccolino et al, 1984; Lasater and Dowling, 1985; Lasater, 1987; DeVries and Schwartz, 1989; McMahon et al, 1989; He et al, 2000).…”

“…In the vertebrate retina, gap junctions are found between virtually every type of neuron, where they function as electrical synapses implicated in several aspects of information processing (Kaneko, 1971; Raviola and Gilula, 1973; Kolb and Famiglietti, 1974; Dowling, 1987; Vaney, 1991; Strettoi et al, 1992; Vaney, 1994; Cook and Becker, 1995). For example, gap junctional coupling between horizontal or amacrine cells is the key component to increase the size of the receptive fields of these cells beyond the limits of their dendritic tree, control spatial resolution and promote synchronized electrical activity in neural networks (Hedden and Dowling, 1978; Negishi and Drujan, 1979; Wässle and Boycott, 1991; Qian and Ripps, 1992; Weiler and Akopian, 1992; Veruki and Hartveit, 2002). It is likely that a dynamic modulation of the lateral spread of signals could influence the integrative properties of these networks of cells, thereby providing a flexible switch between sensitivity and spatial resolution in the rod and cone pathways.…”

Connexin 35: a gap-junctional protein expressed preferentially in the skate retina.

“…These differences seem to depend on the species studied, and on the functional properties of the neural network they subserve. For example, electrical coupling between rod-driven horizontal cells of skate (Qian and Ripps, 1992;Qian et al, 1993) and mammals (Pflug and Nelson, 1993) appears to be relatively insensitive to dopaminergic ligands or any of the intermediaries of the dopamine-activated secondmessenger system that modulate electrical communication between cone-driven horizontal cells of amphibia and some species of fish (Piccolino et al, 1984;Lasater, 1987;DeVries and Schwartz, 1989;McMahon et al, 1989;Dong and McReynolds, 1991). The pharmacological properties of gap junctions between other classes of retinal neurons have not been studied as extensively, but it seems likely that their relative sensitivities to drugs, transmitters, and other agents will be dependent upon similar factors (cf.…”

pH Regulation in Horizontal Cells of the Skate Retina

“…As in all other vertebrate species studied thus far, skate horizontal cells receive direct synaptic input from the photoreceptors, they are depolarized by glutamate and other excitatory amino acids (Dowling and Ripps, 1973 ;Lasater, Dowling and Ripps, 1984), they are strongly coupled via pHsensitive gap junctions (Qian and Ripps, 1992 ;Qian, Malchow and Ripps, 1993), and they display a large complement of voltage-gated membrane channels (Malchow et al, 1990). The approach we have taken is to examine the recovery of pH i from an experimentally-imposed acid load, a fundamental technique that has been successfully applied to the study of pH i regulation in a broad range of tissues (cf.…”