Intrinsic Light Response of Retinal Horizontal Cells of Teleosts

The discovery of intrinsically photosensitive retinal ganglion cells (ipRGCs) has overthrown the long-held belief that rods and cones are the exclusive retinal photoreceptors1, 2. IpRGCs use melanopsin3 as the photopigment, and mediate non-image-forming visual functions such as circadian photoentrainment. In fish, melanopsin has been suggested by in situ hybridization studies to be in retinal horizontal cells (HCs)4-6– lateral association neurons critical for creating the center-surround receptive fields of visual neurons. Are fish HCs, then, possibly also intrinsically photosensitive? This iconoclastic notion was examined previously in flat-mount roach retina, but all HC light response disappeared after synaptic transmission was blocked6, making any conclusion difficult. To directly examine this question, we have now recorded from single, acutely dissociated fish HCs. We found that light induced a response in cone HCs but not rod HCs from catfish, consisting of a modulation of the nifedipine-sensitive, voltage-gated Ca current. The light response was extremely slow, lasting for many minutes. Similar light responses were observed in a high percentage of goldfish HCs. We have cloned from catfish two melanopsin genes and one vertebrate ancient (VA) opsin gene. In situ hybridization indicated that melanopsin, but less likely VA opsin, was expressed in the HC layer of catfish retina. This intrinsic light response may serve to modulate, over a long time scale, lateral inhibition mediated by these cells. Thus, at least in some vertebrates, there are retinal non-rod/non-cone photoreceptors involved primarily in image-forming vision.