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

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Abstract
Electrical coupling via gap junctions is a common property of CNS neurons. In retinal photoreceptors, coupling plays important roles in noise filtering, intensity coding, and spatial processing. In many vertebrates, coupling is regulated during the course of light adaptation. To understand the mechanisms of this regulation, we studied photoreceptor gap junction proteins. We found that two connexins were expressed in bass cone photoreceptors. Connexin 35 (Cx35) mRNA was present in many cell types, including photoreceptors and amacrine, bipolar, and a few ganglion cells. Antibodies to Cx35 labeled abundant gap junctions in both the inner and outer plexiform layers. In the outer plexiform layer, numerous plaques colocalized with cone telodendria at crossing contacts and tip-to-tip contacts. Cx34.7 mRNA was found predominantly in the photoreceptor layer, primarily in cones. Cx34.7 immunolabeling was limited to small plaques immediately beneath cone pedicles and did not colocalize with Cx35. Cx34.7 plaques were associated with a dense complex of cone membrane beneath the pedicles, including apparent contacts between telodendria and cone pedicles. Tracer coupling studies of the connexins expressed in HeLa cells showed that coupling through Cx35 gap junctions was reduced by protein kinase A (PKA) activation and enhanced by PKA inhibition through a greater than fivefold activity range. Cx34.7 was too poorly expressed to study. PKA regulation suggests that coupling through Cx35 gap junctions can be controlled dynamically through dopamine receptor pathways during light adaptation. If Cx34.7 forms functional cell-cell channels between cones, it would provide a physically separate pathway for electrical coupling.