Modulation of cone horizontal cell activity in the teleost fish retina. I. Effects of prolonged darkness and background illumination on light responsiveness

Abstract

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)

Light adaptation affects synaptic vesicle density but not the distribution of GABA A receptors in goldfish photoreceptor terminals

“…3B). This corroborative finding means that during periods of inactivity (prolonged darkness) (Raynauld et al, 1979;Yang et al, 1988), there is a concomitant decrease in synaptic ribbon length and an increase in synaptic vesicle density in goldfish cones.…”

“…With dark adaptation and retraction of the spinules, there may be an increase in the recovery of cone plasma membrane (Wagner, 1980) and a consequent increase in synaptic vesicle density. Also, cone neurotransmission in teleost fish is suppressed markedly during prolonged dark adaptation (e.g., Raynauld et al, 1979;Yang et al, 1988), perhaps resulting in an excess accumulation of synaptic vesicles.…”

Light adaptation and the luminance-response function of the cone electroretinogram

“…3C), most single cell studies of the cone pathway have not reported an increase in response amplitude with increasing levels of light adaptation [11,12]. However, an exception can be found in white perch cone horizontal cells, the responses of which are smallest under conditions of dark adaptation and are enhanced by light adaptation [14,15]. The adaptation-induced enhancement of white perch horizontal cell responses appears to reflect a neuromodulatory influence involving dopamine [15].…”

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].…”

“…This indicates that cone pathways are selectively depressed, and the notion that cone pathways remain fully functional in prolonged darkness may not be correct. In other words, cone horizontal cells require background illumination to maintain high light responsiveness [3].…”