Abstract
Although it is well established that the vertebrate retina contains endogenous circadian clocks that regulate retinal physiology and function during day and night, the processes that the clocks affect and the means by which the clocks control these processes remain unresolved. We previously demonstrated that a circadian clock in the goldfish retina regulates rod-cone electrical coupling so that coupling is weak during the day and robust at night. The increase in rod-cone coupling at night introduces rod signals into cones so that the light responses of both cones and cone horizontal cells, which are post-synaptic to cones, become dominated by rod input. By comparing the light responses of cones, cone horizontal cells and rod horizontal cells, which are post-synaptic to rods, under dark-adapted conditions during day and night, we determined whether the daily changes in the strength of rod-cone coupling could account entirely for rhythmic changes in the light response properties of cones and cone horizontal cells. We report that although some aspects of the day/night changes in cone and cone horizontal cell light responses, such as response threshold and spectral tuning, are consistent with modulation of rod-cone coupling, other properties cannot be solely explained by this phenomenon. Specifically, we found that at night compared to the day the time course of spectrally-isolated cone photoresponses was slower, cone-to-cone horizontal cell synaptic transfer was highly non-linear and of lower gain, and the delay in cone-to-cone horizontal cell synaptic transmission was longer. However, under bright light-adapted conditions in both day and night, cone-to-cone horizontal cell synaptic transfer was linear and of high gain, and no additional delay was observed at the cone-to-cone horizontal cell synapse. These findings suggest that in addition to controlling rod-cone coupling, retinal clocks shape the light responses of cone horizontal cells by modulating cone-to-cone horizontal cell synaptic transmission.
Highlights
The vertebrate retina is able to detect and transmit visual images in a moonless night, in the midday sun, and at all times in between when ambient light intensity varies by more than 10 orders of magnitude [1,2]
This study is based on analyses of the light response properties of cones, cone horizontal cells (cHCs) and rod horizontal cells (rHCs) in freshly isolated, intact goldfish neural retinas maintained by superfusion
The retinal clock controls the light responses of goldfish cones and cHCs but not rHCs
Summary
The vertebrate retina is able to detect and transmit visual images in a moonless night, in the midday sun, and at all times in between when ambient light intensity varies by more than 10 orders of magnitude [1,2]. Circadian clocks orchestrate many aspects of retinal physiology and function on a daily basis, including photoreceptor disc shedding, synthesis of dopamine and the neurohormone melatonin, transcriptional activity, and visual sensitivity [3,4,5,6,7,8] Despite this large body of research, the physiological processes that the retinal clocks affect during day and night and the means by which the clocks control these processes remain unresolved. The resultant cone photovoltage controls the opening probability of the voltage-gated calcium channels at the cone pedicle and thereby synaptic transmission between cones and second-order neurons such as bipolar and horizontal cells [1,2]
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