The effects of prolonged (greater than 2 hr) darkness and background illumination on the light responsiveness of cone horizontal cells were examined in isolated, superfused white perch retinas. In retinas from fish maintained in complete darkness for more than 2 hr, cone horizontal cells had a resting membrane potential of about -18 mV, and they generated only slow, low-amplitude (3-4 mV) responses even when stimulated with bright flashes. Following the presentation of dim background light, the cone horizontal cells slowly hyperpolarized and thereafter remained at a more hyperpolarized level (about -25 mV). Concurrently, their light responses were dramatically enhanced in size, and response amplitudes to bright flashes eventually increased to about 50 mV. This was accompanied by noticeable changes in response waveforms; following light exposure, the responses became faster and showed initial on-transients. The increase in cone horizontal cell responsiveness was graded with intensity of the background light. A similar enhancement in response amplitudes of cone horizontal cells occurred after presenting bright flashes repetitively at intervals of 9 sec. This background sensitization phenomenon was observed in both L- and C-type cone horizontal cells. When light-sensitized isolated retinas were maintained in darkness for long periods (greater than 30 min), the light responsiveness of cone horizontal cells gradually decreased. The changes in membrane potential and response waveform were opposite to those that occurred when prolonged dark-adapted retinas were exposed to background lights; the cells depolarized by 5-7 mV and light-evoked responses became slower. Effects of background illumination on rod-driven horizontal cells were examined as well. Rod horizontal cells were about 2 log units more sensitive to white light than were cone horizontal cells. When recorded in prolonged dark-adapted retinas, rod horizontal cells showed large responses (approximately 50 mV), which could not be further enhanced by background illumination. Cone horizontal cell responsiveness in the carp retina was also depressed by prolonged darkness and increased by illumination in a fashion similar to that observed in the white perch retina. The change in response amplitude was only about 2-fold in carp compared with 5- to 10-fold changes observed in white perch. These results indicate that the light responsiveness of cone horizontal cells in the teleost retina is suppressed in prolonged darkness and that background lights release the cells from suppression.(ABSTRACT TRUNCATED AT 400 WORDS)
The effects of prolonged darkness and dopamine on the coupling between horizontal cells in the isolated, superfused white perch retina were studied. Two assays of coupling were employed; area versus amplitude relationships (area-response curves) and the diffusion of the fluorescent dye Lucifer yellow from intracellularly injected cells to neighboring cells. In prolonged dark-adapted retinas, area-response curves were difficult to determine because of the small light responses; however, light-evoked responses did not increase in size when light spots were larger than 0.8 mm in diameter. Following the presentation of dim background illumination that partially sensitized the retina, responses to light spots of various sizes were enhanced and an area-response curve could be constructed. Subsequent presentation of moderate background illumination that more fully sensitized the retina resulted in reduced responses to small spots (less than 1.6 mm in diameter) and enhanced responses to large spot or full-field stimuli. In retinas exposed to moderate background illumination, Lucifer yellow injected intracellularly into cone horizontal cells diffused into many neighboring horizontal cells. The coupled cells were very similar in morphology, suggesting they were of the same type. In prolonged dark-adapted retinas, on the other hand, the dye was usually restricted to the injected cell and a few adjacent cells. These results indicate that coupling between cone horizontal cells is modulated by prolonged darkness and background illumination. Following dopamine (50 microM) application, in both 6-OHDA-treated and untreated retinas, changes in area-response curves of cone horizontal cells were observed just opposite to those that occurred when prolonged dark-adapted retinas were exposed to background illumination. That is, following 5 min application of dopamine to the retina, responses to small spots (less than 2 mm in diameter) increased in size while responses to larger spots decreased in amplitude compared with control responses. Following 20 min of superfusion with dopamine, the recorded responses were very small, and an accurate area-response curve could not be determined. Following dopamine application to light-sensitized retinas, Lucifer yellow was restricted to the injected cells or to the injected cell and a few neighboring cells. The results suggest that the modulation of coupling between cone horizontal cells by prolonged darkness and background illumination may be mediated by dopamine. Spatial properties of rod horizontal cells were also examined.(ABSTRACT TRUNCATED AT 400 WORDS)
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.
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