Intrinsic light response of retinal horizontal cells of teleosts

The discovery of intrinsically photosensitive retinal ganglion cells has overthrown the long-held belief that rods and cones are the exclusive retinal photoreceptors(1,2). Intrinsically photosensitive retinal ganglion cells use melanopsin(3) as the photopigment, and mediate non-image-forming visual functions such as circadian photoentrainment. In fish, in situ hybridization studies indicated that melanopsin is present in retinal horizontal cells(4-6)-lateral association neurons critical for creating the centre-surround receptive fields of visual neurons. This raises the question of whether fish horizontal cells are intrinsically photosensitive. This notion was examined previously in flat-mount roach retina, but all horizontal-cell light response disappeared after synaptic transmission was blocked(6), making any conclusion difficult to reach. To examine this question directly, we have now recorded from single, acutely dissociated horizontal cells from catfish and goldfish. We found that light induced a response in catfish cone horizontal cells, but not rod horizontal cells, consisting of a modulation of the nifedipine-sensitive, voltage-gated calcium current. The light response was extremely slow, lasting for many minutes. Similar light responses were observed in a high percentage of goldfish horizontal cells. We have cloned two melanopsin genes and one vertebrate ancient (VA) opsin gene from catfish. In situ hybridization indicated that melanopsin, but less likely VA opsin, was expressed in the horizontal-cell 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.