Abstract
Continuous visual perception and the dark adaptation of vertebrate photoreceptors after bright light exposure require recycling of their visual chromophore through a series of reactions in the retinal pigmented epithelium (RPE visual cycle). Light-driven chromophore consumption by photoreceptors is greater in daytime vs. nighttime, suggesting that correspondingly higher activity of the visual cycle may be required. However, as rod photoreceptors are saturated in bright light, the continuous turnover of their chromophore by the visual cycle throughout the day would not contribute to vision. Whether the recycling of chromophore that drives rod dark adaptation is regulated by the circadian clock and light exposure is unknown. Here, we demonstrate that mouse rod dark adaptation is slower during the day or after light pre-exposure. This surprising daytime suppression of the RPE visual cycle was accompanied by light-driven reduction in expression of Rpe65, a key enzyme of the RPE visual cycle. Notably, only rods in melatonin-proficient mice were affected by this daily visual cycle modulation. Our results demonstrate that the circadian clock and light exposure regulate the recycling of chromophore in the RPE visual cycle. This daily melatonin-driven modulation of rod dark adaptation could potentially protect the retina from light-induced damage during the day.
Highlights
IntroductionThe visual pigments in rods and cones are photobleached at a high rate, whereas a minimal amount of chromophore is used and recycled at night
(A) Representative dark-adapted scotopic in vivo ERG responses to various light intensities from melatoninproficient C3H/f+/+ mice. (B) Representative dark-adapted scotopic in vivo ERG responses from melatoninproficient CBA/CaJ mice revealing b-wave deficit. (C) Normalized in vivo ERG scotopic a-wave maximal response (a-wave rmax/rDAmax) recovery in C3H/f+/+ mice following 90% pigment bleach at t = 0 at subjective night and subjective day (*p < 0.05). (D) Normalized in vivo ERG scotopic a-wave sensitivity (a-wave Sf/a-wave SfDA) recovery in C3H/f+/+ mice following 90% pigment bleach at t = 0 at subjective night and subjective day (*p < 0 .05)
In order to determine whether pigment regeneration is regulated by the circadian clock, we examined the kinetics of rod dark adaptation in C3H/f+/+ mice in subjective night and subjective day
Summary
The visual pigments in rods and cones are photobleached at a high rate, whereas a minimal amount of chromophore is used and recycled at night This day/night difference in chromophore consumption prompted us to ask: is pigment regeneration under the regulation of the circadian clock, in accordance with chromophore demand? We addressed these questions by electrophysiological recordings and molecular analysis of retinas of melatonin-proficient (C3H/f+/+ and CBA/CaJ) and melatonin-deficient (C57BL/6J and 129S2/Sv) mouse strains
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