Dopamine mediates circadian clock regulation of rod and cone input to fish retinal horizontal cells

Abstract

A circadian (24-hour) clock regulates the light responses of fish cone horizontal cells, second order neurones in the retina that receive synaptic contact from cones and not from rods. Due to the action of the clock, cone horizontal cells are driven by cones in the day, but primarily driven by rods at night. We show here that dopamine, a retinal neurotransmitter, acts as a clock signal for the day by increasing cone input and decreasing rod input to cone horizontal cells. The amount of endogenous dopamine released from in vitro retinae was greater during the subjective day than the subjective night. Application of dopamine or quinpirole, a dopamine D 2 -like agonist, during the subjective night increased cone input and eliminated rod input to the cells, a state usually observed during the subjective day. In contrast, application of spiperone, a D 2 -like antagonist, or forskolin, an activator of adenylyl cyclase, during the subjective day reduced cone input and increased rod input. SCH23390, a D 1 antagonist, had no effect. Application of R p -cAMPS, an inhibitor of cAMPdependent protein kinase, or octanol, an alcohol that uncouples gap junctions, during the night increased cone input and decreased rod input. Because D 2 -like receptors are on photoreceptor cells, but not horizontal cells, the results suggest that the clock-induced increase in dopamine release during the day activates D 2 -like receptors on photoreceptor cells. The resultant decrease in intracellular cyclic AMP and protein kinase A activation then mediates the increase in cone input and decrease in rod input.

Olfactory input increases visual sensitivity in zebrafish: a possible function for the terminal nerve and dopaminergic interplexiform cells

“…Interestingly, retinal GnRH content depends on diurnal and seasonal factors and on the state of light/dark-adaptation (Ball et al, 1989). We found that olfactory stimulation increased visual sensitivity only in the early morning, not in the late afternoon when visual sensitivity and retinal dopamine release are already high (Li and Dowling, 1998;Ribelayga et al, 2002). This shift of visual sensitivity from an early morning state to a late afternoon state could be blocked by a dopamine D2 antagonist.…”

“…Dopamine release is under the control of light (Weiler et al, 1997;Kirsch and Wagner, 1989) and a circadian clock (Doyle et al, 2002;Ribelayga et al, 2002). Although many questions remain about the mechanism of retinal dopamine functions, one of the main pictures emerging is that dopamine plays a role in the modulation of neural circuitry during light and dark adaptation (Dowling, 1986;Witkovsky and Dearry, 1992).…”

Cone Photoreceptors in Bass Retina Use Two Connexins to Mediate Electrical Coupling

“…In contrast, rod-cone coupling is thought to decrease with dopamine D 2 -like receptor activation or light sensitization in goldfish (Wang and Mangel, 1996;Ribelayga et al, 2002). Such differences highlight the precise nature with which photoreceptor coupling is controlled in each species.…”

“…Rod-cone gap junctions have been observed in most species, and indirect evidence exists for electrical coupling between rods and cones in fish (Ribelayga et al, 2002). It is logical to expect one of connexins 35 and 34.7 to mediate this coupling.…”

A neuromorphic model for achromatic and chromatic surface representation of natural images

“…These processes include light adaptation and contrast adaptation. Some retinal mechanisms contributing to these adaptations include: (1) Ca 2 + ion-mediated negative feedback occurring at the photoreceptors (Koutalos & Yau, 1996) and bipolar cells (Nawy, 2000); (2) bleaching of photopigments (Dowling, 1987;Fain, 2001); (3) surround negative feedback by the horizontal cell (HC) network (Lee et a!., 1999;McMahon et a!., 2001;Sterling, 1998~ Thibos & Werblin, 1978Werblin, 1974); and (4) a circuitry switch from cones to rods (Mills & Massey, 1995;Ribelayga, Wang & Mangel, 2002). Such mechanisms enable cells to dynamically change their operating range to adapt to varying lighting situations.…”