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Intrinsic light response of retinal horizontal cells of teleosts

Nature volume 460, pages 899–903 (2009)Cite this article

Abstract

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.

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Figure 1: Light modulated the voltage-gated Ca 2+ current on catfish cone horizontal cells.
Figure 2: Characterization of catfish cone horizontal-cell light response.
Figure 3: Melanopsin, but perhaps not VA/VAL opsin, was expressed in the horizontal cell layer of catfish retina.
Figure 4: Many goldfish horizontal cells also showed light responses.

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Acknowledgements

This work was supported by an NIH grant and the António Champalimaud Vision Award (Portugal) to K.-W.Y. We thank R. Johnson, C. Liu and D. Liu for advice on molecular cloning and in situ hybridization staining, Y. Shen, C. Linn and G. Matthews for suggestions on retinal dissociation. D. Bergles, P. Fuchs and J. Nathans offered comments throughout the work. L. Belluscio let N.C. take a brief leave of absence from her postdoctoral work to return to Hopkins in order to complete some experiments. Members of the Yau laboratory, especially M. Do and D.-G. Luo, as well as K. Murari, have provided comments on the manuscript.

Author Contributions N.C., T.T. and K.-W.Y. discussed and designed the experiments. N.C. performed all of the experiments, with T.T. offering technical advice. N.C. and K.-W.Y. wrote the paper.

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  1. Ning Cheng & Takashi Tsunenari

    Present address: Present addresses: Unit of Developmental Neural Plasticity, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892, USA (N.C.); Graduate Program of Human Sensing and Functional Sensor Engineering, Graduate School of Science and Engineering, Yamagata University, Yonezawa City, Yamagata 992-8510, Japan (T.T.).,

Authors and Affiliations

  1. Solomon H. Snyder Department of Neuroscience,,

    Ning Cheng, Takashi Tsunenari & King-Wai Yau

  2. Center for Sensory Biology and,,

    Ning Cheng, Takashi Tsunenari & King-Wai Yau

  3. Department of Ophthalmology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205, USA,

    King-Wai Yau

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  1. Ning Cheng
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Correspondence to Ning Cheng or King-Wai Yau.

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Cheng, N., Tsunenari, T. & Yau, KW. Intrinsic light response of retinal horizontal cells of teleosts. Nature 460, 899–903 (2009). https://doi.org/10.1038/nature08175

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