Dopamine D2 receptor‐mediated modulation of rod‐cone coupling in the Xenopus retina

Abstract

We studied the responses of rod photoreceptors that were elicited with light flashes or sinusoidally modulated light by using intracellular recording. Dark-adapted Xenopus rod photoreceptors responded to sinusoidally modulated green lights at temporal frequencies between 1 Hz and 4 Hz. In normal Ringer's solution, 57% of the rods tested could follow red lights that were matched for equal rod absorbance to frequencies >5 Hz, indicating an input from red-sensitive cones. Quinpirole (10 μM), a D2 dopamine agonist, increased rod-cone coupling, whereas spiperone (5 μM), a selective D2 antagonist, completely suppressed it. D1 dopamine ligands were without effect. Neurobiotin that was injected into single rods diffused into neighboring rods and cones in quinpirole-treated retinas but only diffused into rods in spiperone-treated retinas. A subpopulation of rods (ca. 10% total rods) received a very strong cone input, which quickened the kinetics of their responses to red flashes and greatly increased the bandpass of their responses to sinusoidally modulated light. Based on electron microscopic examination, which showed that rod-rod and cone-cone gap junctions are common, whereas rod-cone junctions are relatively rare, we postulate that cone signals enter the rod network through a minority of rods with strong cone connections, from which the cone signal is further distributed in the rod network. A semiquantitative model of coupling, based on measures of gapjunction size and distribution and estimates of their conductance and open times, provides support for this assumption. The same network would permit rod signals to reach cones. Keywords gap junction; photoreceptor; retina; neuromodulation When rod photoreceptors are fully dark-adapted, they respond reliably to the absorbance of a single quantum of light (Yau et al., 1977). Rods continue to function when they are desensitized by background lights (Fain, 1976) or by prior exposure to light, and, in those circumstances, the effective stimuli for rods can be sufficiently bright to also activate cone photoreceptors, allowing for the possibility of interactions between rod signals and cone signals. (Raviola and Gilula, 1973), and functional rod-cone coupling in primate retina has been reported (Schneeweis and Schnapf, 1995).The main experimental question of the present study is whether the conductances of photoreceptor gap junctions are subject to neuromodulation. We focus on the intrinsic retinal neurochemical, dopamine (Haggendal and Malmfors, 1965), which is known to modulate the gap-junctional conductance of retinal second-order neurons (Piccolino et al., 1984) and to augment information flow in cone circuits while suppressing that in rod circuits (Witkovsky and Dearry, 1991). Photoreceptors have dopamine receptors of the D2/D4 subtypes (Cohen et al., 1992;Muresan and Besharse, 1993). In the present study, we found that a D2 dopamine agonist, but not a D1 agonist, increases rod-cone coupling in the Xenopus retina, resulting in altered rod light-evoked response k...

Synaptic transmission at retinal ribbon synapses

“…In the cone circuit, noise is reduced by utilizing desensitized AMPA/KA receptors (De Vries and Schwartz, 1999). Voltage noise in amphibian, but not mammalian rod is reduced by rod-rod coupling (Krizaj et al, 1998;Schneeweis and Schnapf, 1995), but this does not greatly diminish the noisy Ca 2+ signals arising from stochastic openings of single calcium channels. Pooling of noisy signals through integration within the OFF bipolar cell dendrites, however, does occur in all vertebrate retinas.…”

Rod and Cone Contributions to Horizontal Cell Light Responses in the Mouse Retina

“…Interaction between the rod and cone pathways is extensive: rods and cones are electrically coupled (Raviola and Gilula, 1973;Smith et al, 1986;Schneeweis and Schnapf, 1995;Krizaj et al, 1998;Tsukamoto et al, 2001), and rod signals piggyback onto cone pathways at several stages in visual processing (for review, see Völgyi et al, 2004). This interaction of the two photoreceptor systems is essential for adaptation of photoreceptor sensitivity to different levels of ambient illumination.…”

Connexin 35/36 is phosphorylated at regulatory sites in the retina

“…For example, gap junctions between photoreceptors spread responses through adjacent terminals, improving the signal:noise ratio under many conditions (Schwartz, 1975b;Lamb & Simon, 1976), and expanding the voltage range through which a synaptic response is possible (Attwell et al, 1987). Rod-cone gap junctions also provide a pathway through which high-sensitivity rod signals may enter the cone pathways and chromatic or high frequency cone signals may enter the rod pathway (Schwartz, 1975a;Wu & Yang, 1988;Krizaj et al, 1998).…”

“…The effect of light on photoreceptors is partially mimicked by dopamine D2/D4-like receptor activation (Krizaj et al, 1998), which results in reduction of adenylyl cyclase activity and cytoplasmic cAMP concentration (Cohen et al, 1992;Nir et al, 2002). In other retinal networks, the opposite effect is mediated by dopamine D1-type receptors.…”