Intrinsic light response of retinal horizontal cells of teleosts

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Abstract
It has recently become apparent that the familiar rods and cones are not the only photoreceptors in mammals — a third class known as intrinsically photosensitive retinal ganglion cells (ipRGCs) are now known to relay light information that synchronizes circadian rhythms and triggers the papillary light reflex. Here, Cheng et al. show that a subset of retinal horizontal cells in teleost fish is also photosensitive. Like mammalian ipRGCs, the photopigment that confers photosensitivity in this subset of vertebrate horizontal cells appears to be melanopsin. It has recently become apparent that rods and cones are not the only photoreceptors in mammals. A third class, known as intrinsically photosensitive retinal ganglion cells, use the photopigment melanopsin and mediate non-image-forming visual functions such as circadian photoentrainment. In teleost fish, a subset of horizontal cells is now shown to be photosensitive; the photopigment responsible for this seems to be melanopsin. The discovery of intrinsically photosensitive retinal ganglion cells has overthrown the long-held belief that rods and cones are the exclusive retinal photoreceptors1,2. Intrinsically photosensitive retinal ganglion cells use melanopsin3 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 cells4,5,6—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 blocked6, 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 timescale, 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.