Modulation of cone horizontal cell activity in the teleost fish retina. II. Role of interplexiform cells and dopamine in regulating light responsiveness

Abstract

Following the destruction of the terminals of the dopaminergic interplexiform cells by intraocular injections of 6-hydroxydopamine (6-OHDA), cone horizontal cells exhibited high light responsiveness in prolonged darkness and their responses to moderate and bright full-field flashes were as large as 60 mV. Furthermore, the light responsiveness of these cells in the 6-OHDA-treated retinas was not enhanced by background illumination. The application of dopamine (50 microM) by superfusion to 6-OHDA-treated retinas resulted in a decrease in light responsiveness and changes in response waveform of the cone horizontal cells. Twenty minutes following dopamine application the responses of the cone horizontal cells closely resembled the response of cells recorded in prolonged dark-adapted retinas. Dopamine caused similar changes in cone horizontal cells recorded in light-exposed retinas, but had no obvious effects on rod horizontal cells. The selective dopamine D1 receptor antagonist, Sch 23390, enhanced cone horizontal cell responsiveness when applied to prolonged dark-adapted retinas, mimicking background illumination. The light responsiveness of cone horizontal cells recorded after application of Sch 23390 was less than that for cells in retinas that had been exposed to background lights, but light responsiveness could not be further enhanced by background illumination. Another dopamine antagonist, (+)-butaclamol, was found to have effects similar to Sch 23390 on cone horizontal cells, but (-)-butaclamol, the inactive enantiomer, did not enhance the light responsiveness of these cells. The results suggest that the dopaminergic interplexiform cells play a crucial role in the regulation of cone horizontal cell responsiveness by prolonged darkness and background illumination. These cells may release dopamine tonically in the dark, which suppresses cone horizontal cell responsiveness. Background illumination may decrease dopamine release and liberate cone horizontal cells from the suppression.

Dopamine enhances a glutamate-gated ionic current in OFF bipolar cells of the tiger salamander retina

“…For example, al- Maguire and Werbl i n -Dopamine-Glutamate Receptor Interactions ready we know that the GluR l-GluR4 subunits lack consensus phosphorylation sites for PKA, while GluR6 does contain such a site (Raymond et al, 1993 Recent studies indicate a diversity of glutamate receptors in the outer retina (Nawy and Jahr, 1990;Shiells and Falk, 1990;Gilbertsen et al, 199 1;Hirano and MacLeish, 199 1;Hughes et al, 1992;Hamasaki-Britto et al, 1993), and suggest that separate populations of glutamate receptors on bipolar (Nawy and Copenhagen, 1987) and horizontal cells (Kim and Miller, 1992) may be differentially sensitive to rod and cone input. The studies of Dowling and coworkers (Yang et al, 1988) indicate that glutamate receptors on cone horizontal cells are upmodulated by dopamine, while those on rod horizontal cells are unaffected. The bipolar cells in this study probably receive both rod and cone inputs (Hare et al, 1986), but dopamine may regulate only those receptors associated with cones.…”

“…[Key words: vision, retina, glutamate receptors, dopamine, bipolar cell, modulation] Recent evidence suggests that dopamine is an endogenous transmitter in retinal interplexiform cells (Dowling and Ehinger, 1975) and amacrine cells (Brecha et al, 1984;Witkovsky et al, 1984;Yang et al, 1991) and that its rate of release is controlled by light or dark stimulation and by circadian rhythms (Besharse et al, 1988;Witkovsky and Dearry, 1992;Witkovsky et al, 1993). Dopamine application to the retina has been shown to increase the contribution of cone input to cells in the outer (Yang et al, 1988;Witkovsky et al, 1989) and inner retina (Maguire and Hamasaki, 1993), and to modulate the surround inhibition mediated by horizontal cells (Mange11 and . Dopamine may modify the coupling through gap junctions between horizontal cells (Piccolino et al, 1984;Lasater and Dowling, 1985) and may also modulate the sensitivity of glutamate receptors on horizontal cells (Knapp and Dowling, 1987).…”

Dopamine and serotonin turnover rate in the retina of rabbit, rat, goldfish, and Eugerres plumieri: Light effects in goldfish and rat

“…Retina contains the enzymes for the synthesis of DA, tyrosine hydroxylase (TH) and aromatic L-amino acid decarboxylase (Iuvone et al, 1978a,b;Iuvone, 1984;Parkinson et al, 1985;Yang et al, 1988). Much evidence supports the role of DA in the light-evoked response.…”

Modulation of synaptic transmission in the retina

“…Intracellular responses of horizontal cells and electroretinographic (ERG) responses were simultaneously recorded and conventionally analyzed. In some eases, Lucifer yellow was intracellularly injected to monitor dye coupling between horizontal cells by gap junctions [3,4].…”

“…The roles of dopaminergic interplexiform cells in the regulation of light responsiveness of cone horizontal cells and coupling between them by prolonged darkness and background illumination have been extensively examined [4]. Interplexiform cells are retinal neurons whose perikarya are located among the amacrine cells and that send processes to the outer plexiform layer where they make numerous synapses onto the cone horizontal cells [8,9].…”