The discovery of intrinsically photosensitive retinal ganglion cells (ipRGCs) has overthrown the long-held belief that rods and cones are the exclusive retinal photoreceptors. IpRGCs use melanopsin as the photo pigment, which, in fish, has been suggested by in situ hybridization studies to be in retinal horizontal cells (HCs)---lateral association neurons critical for creating the center-surround receptive fields of bipolar cells. Are fish HCs, then, possibly also intrinsically photosensitive? This iconoclastic notion was examined previously in flat-mount roach retina, but the supposedly intrinsic light response disappeared after synaptic transmission was blocked. To directly examine this question, we have now recorded from single, acutely dissociated fish HCs. We found that light induced an electrical response in a substantial percentage of cone HCs from catfish, but not in rod HCs, consisting of a modulation of the nifedipine-sensitive, voltage-gated Ca current. This effect seemed specific; for example, voltage-gated Na and K currents as well as glutamate- and gamma-aminobutyric-acid-induced currents of cone HCs were not affected by light. The light response was extremely slow, lasting for many minutes. Similar light responses were also observed in goldfish HCs. The intrinsic spectral sensitivity of the catfish cone HCs peaked at between 440 nm and 520 nm. Melanopsin, but not vertebrate ancient (VA) opsin, messenger RNA was found expressed in the horizontal cell layer of catfish retina, suggesting melanopsin is possibly the underlying photo pigment. This intrinsic light response may serve to modulate, over a long time scale, lateral inhibition mediated by fish cone HCs.
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