Abstract
BackgroundAlthough the circadian clock in the mammalian retina regulates many physiological processes in the retina, it is not known whether and how the clock controls the neuronal pathways involved in visual processing.Methodology/Principal FindingsBy recording the light responses of rabbit axonless (A-type) horizontal cells under dark-adapted conditions in both the day and night, we found that rod input to these cells was substantially increased at night under control conditions and following selective blockade of dopamine D2, but not D1, receptors during the day, so that the horizontal cells responded to very dim light at night but not in the day. Using neurobiotin tracer labeling, we also found that the extent of tracer coupling between rabbit rods and cones was more extensive during the night, compared to the day, and more extensive in the day following D2 receptor blockade. Because A-type horizontal cells make synaptic contact exclusively with cones, these observations indicate that the circadian clock in the mammalian retina substantially increases rod input to A-type horizontal cells at night by enhancing rod-cone coupling. Moreover, the clock-induced increase in D2 receptor activation during the day decreases rod-cone coupling so that rod input to A-type horizontal cells is minimal.Conclusions/SignificanceConsidered together, these results identify the rod-cone gap junction as a key site in mammals through which the retinal clock, using dopamine activation of D2 receptors, controls signal flow in the day and night from rods into the cone system.
Highlights
The remarkable ability of the vertebrate retina to adapt to the,109–fold range of light intensities that spans a moonless night and a bright sunny day relies on a complex interplay between responses to the mean background illumination and signals originating from an endogenous circadian (24-h) clock [1,2,3]
The circadian clock in the mammalian retina regulates many physiological processes in the retina, including increasing dopamine release in the day [2,4,5], it is not known whether and how the clock controls the neuronal pathways involved in visual processing in the day and night
Circadian clock control of the light responses of rabbit Atype horizontal cells The light responses of A-type horizontal cells in superfused rabbit retinas were studied under thoroughly dark-adapted conditions during the subjective day (circadian time (CT)2–10) and subjective night (CT14–22) of a circadian cycle and during the day (zeitgeber time (ZT)2–10) and night (ZT14–22) of a regular light-dark cycle [see Materials and Methods]
Summary
The remarkable ability of the vertebrate retina to adapt to the ,109–fold range of light intensities that spans a moonless night and a bright sunny day relies on a complex interplay between responses to the mean background illumination and signals originating from an endogenous circadian (24-h) clock [1,2,3]. The circadian clock in the mammalian retina regulates many physiological processes in the retina, including increasing dopamine release in the day [2,4,5], it is not known whether and how the clock controls the neuronal pathways involved in visual processing in the day and night. Due to the clock-induced increase in the conductance of the electrical synapses between rods and cones at night, fish cones can respond to very dim light stimuli (scotopic range, see definition in Materials and Methods) because of the signals they receive from coupled rods [6] and can transmit these signals to cone-connected horizontal cells [7], a type of second-order neuron that is postsynaptic to cones, but not to rods [9,10]. The circadian clock in the mammalian retina regulates many physiological processes in the retina, it is not known whether and how the clock controls the neuronal pathways involved in visual processing
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