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GABA-like immunoreactivity in the developing chick retina: differentiation of GABAergic horizontal cell and its possible contacts with photoreceptors

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Journal of Neurocytology

Summary

The morphology of γ-aminobutyric acid (GABA)-containing horizontal cells was examined in mature and developing chick retinas by GABA immunocytochemistry. In the outer plexiform layer of the mature retina, GABA-immunoreactive components were located in three different sublayers. In the inner (vitreal) layer most positively-stained fibres were laterally oriented processes from horizontal cells. Thick processes were found in the middle layer, and the relatively thin fibres in the outer (scleral) layer showed a concave curvature, suggesting their termination on photoreceptor terminals. By electron microscopy it was found that the principal cone pedicles were usually indented by immunoreactive lateral neurites of horizontal cells but that rod spherules faced only occasionally immunoreactive fibres. Accessory cones and single cones were also not usually indented by immunoreactive fibres. These observations may indicate that horizontal cells regulate the excitation of cone photoreceptors by several different inhibitory mechanisms. During retinal development, horizontal cells begin to extend lateral fibres by the ninth embryonic day, and some GABAergic horizontal cells also possess inwardly extending fibres until embryonic day 11. Between embryonic days 13 and 15, some immunoreactive cells were found among the bipolar cells, suggesting that they were still migrating to their final position. On embryonic day 17, the staining pattern was very similar to that of the mature retina. These results suggest that GABA immunohistochemistry may be an excellent tool for studying horizontal cell differentiation.

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References

  • Agardh, E., Bruun, A., Ehinger, B. &Stormmathisen, J. (1986) Gaba immunoreactivity in the retina.Investigative Ophthalmology and Visual Science 27, 674–8.

    Google Scholar 

  • Agardh, E., Bruun, A., Ehinger, B., Ekstrom, P., Van Veen, T. &Wu, J.-Y. (1987) Gamma-aminobutyric acid- and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates.Journal of Comparative Neurology 258, 622–30.

    Google Scholar 

  • Araki, M., Fukada, Y., Shichida, Y. &Yoshizawa, T. (1990) Immunocytochemical localization of iodopsin in the chick retina duringin vivo andin vitro cone differentiation.Investigative Ophthalmology and Visual Science 31, 1466–73.

    Google Scholar 

  • Araki, M., Maeda, T. &Kimura, H. (1983) Dopaminergic cell differentiation in the developing chick retina.Brain Research Bulletin 10, 97–102.

    Google Scholar 

  • Araki, M. &Saito, T. (1983) Electron microscopic histochemistry of alkaline phosphatase activity in the developing chick retina.Experimental Eye Research 36, 187–98.

    Google Scholar 

  • Ball, A. K. (1987) Immunocytochemical and autoradiographic localization of GABAergic neurons in the goldfish retina.Journal of Comparative Neurology 255, 317–25.

    Google Scholar 

  • Brandon, C. (1985) Retinal GABA neurons: localization in vertebrate species using an antiserum to rabbit brain glutamate decarboxylase.Brain Research 344, 286–95.

    Google Scholar 

  • Brecha, N. (1983) Retinal neurotransmitters: histochemical and biochemical studies. InClinical Neuroanatomy (edited byEmson, P. C.) pp. 85–129. New York: Raven Press.

    Google Scholar 

  • Chun, M. H. &Wässle, H. (1989) GABA-like immunoreactivity in the cat retina: electron microscopy.Journal of Comparative Neurology 279, 55–67.

    Google Scholar 

  • Frederick, J. M. (1987) The emergence of GABA-accumulating neurons during retinal histogenesis in the embryonic chick.Experimental Eye Research 45, 933–45.

    Google Scholar 

  • Hinds, J. W. &Hinds, P. L. (1979) Differentiation of photoreceptors and horizontal cells in the embryonic mouse retina: an electron microscopic, serial section analysis.Journal of Comparative Neurology 187, 495–512.

    Google Scholar 

  • Hollyfield, J. G., Rayborn, M. E., Sarthy, P. V. &Lam, D. M. K. (1979) The emergence, localization and maturation of neurotransmitter systems during development of the retina inXenopus laevis.Journal of Comparative Neurology 188, 587–98.

    Google Scholar 

  • Hsu, S.-M., Raine, L. &Fanger, H. (1981) Use of avidinbiotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody (PAP) procedures.Journal of Histochemistry and Cytochemistry 29, 577–80.

    Google Scholar 

  • Kolb, H. &Jones, J. (1984) Synaptic organization of the outer plexiform layer of the turtle retina: an electron microscope study of serial sections.Journal of Neurocytology 13, 567–91.

    Google Scholar 

  • Lam, D. M. K., Lasater, E. M. &Naka, K. (1978) γ-aminobutyric acid: a neurotransmitter candidate for cone horizontal cells of the catfish retina.Proceedings of National Academy of Sciences (USA) 75, 6310–13.

    Google Scholar 

  • Lam, D. M. K., Thomas Su, Y. Y., Swain, L., Marc, R. E., Brandon, C. &Wu, J.-Y. (1979) Immunocytochemical localization of L-glumatic acid decarboxylase in the goldfish retina.Nature 278, 565–7.

    Google Scholar 

  • Lane, B. P. &Europa, D. L. (1965) Differential staining of ultrathin sections of Epon-embedded tissues for light microscopy.Journal of Histochemistry and Cytochemistry 13, 579–82.

    Google Scholar 

  • Leeper, H. F. (1978) Horizontal cells of the turtle retina. II. Analysis of interconnections between photoreceptor cells and horizontal cells by light microscopy.Journal of Comparative Neurology 182, 795–810.

    Google Scholar 

  • McLaughlin, B. J. (1976) A fine structural and E-PTA study of photoreceptor synaptogenesis in the chick retina.Journal of Comparative Neurology 170, 347–64.

    Google Scholar 

  • Marc, R. E., Stell, W. K., Bok, D. &Lam, D. M. K. (1978) GABAergic pathways in the goldfish retina.Journal of Comparative Neurology 182, 221–46.

    Google Scholar 

  • Marshall, J. &Voaden, M. (1974) An autoradiographic study of the cells accumulating3H-γ-aminobutyric acid in the isolated retinas of pigeons and chickens.Investigative Ophthalmology and Visual Science 13, 602–7.

    Google Scholar 

  • Meller, K. &Tetzlaff, W. (1977) The development of membrane specializations, in the receptor-bipolar-horizontal cell synapse of the chick embryo retina.Cell and Tissue Research 181, 319–26.

    Google Scholar 

  • Morris, V. M. (1970) Symmetry in a receptor mosaic demonstrated in the chick from the frequencies, spacing and arrangement of the types of retinal receptor.Journal of Comparative Neurology 140, 359–98.

    Google Scholar 

  • Morris, V. M. &Shorey, C. D. (1967) An electron microscopic study of types of receptor in the chick retina.Journal of Comparative Neurology 129, 313–40.

    Google Scholar 

  • Mosinger, J. L. &Yazulla, S. (1985) Co-localization of GAD-like immunoreactivity and3H-GABA uptake in amacrine cells of rabbit retina.Journal of Comparative Neurology 240, 396–406.

    Google Scholar 

  • Mosinger, J. L., Yazulla, S. &Studholme, K. M. (1986) GABA-like immunoreactivity in the vertebrate retina: a species comparison.Experimental Eye Research 42, 631–44.

    Google Scholar 

  • Nishimura, Y., Schwartz, M. L. &Rakic, P. (1986) GABA and GAD immunoreactivity of photoreceptor terminals in primate retina.Nature 320, 753–6.

    Google Scholar 

  • Onteniente, B., Tago, H., Kimura, H. &Maeda, T. (1986) Distribution of γ-aminobutyric acid-immunoreactive neurons in the septal region of the rat brain.Journal of Comparative Neurology 248, 422–30.

    Google Scholar 

  • Osborn, N. N., Patel, S., Beaton, D. W. &Neuhoff, V. (1986) GABA neurons in retinas of different species and their postnatal developmentin situ and in culture in the rabbit retina.Cell and Tissue Research 243, 117–23.

    Google Scholar 

  • Schabtach, E. &Parkening, T. A. (1974) A method for sequential high resolution light and electron microscopy of selected areas of the same material.Journal of Cell Biology 61, 261–4.

    Google Scholar 

  • Schnitzer, J. &Rusoff, A. C. (1984) Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages.Journal of Neuroscience 12, 2948–55.

    Google Scholar 

  • Stell, W. K., Lightfoot, D. O., Wheeler, T. G. &Leeper, H. F. (1975) Goldfish retina: functional polarization of cone horizontal cell dendrites and synapses.Science 190, 989–90.

    Google Scholar 

  • Tachibana, M. &Kaneko, A. (1984) γ-aminobutyric acid acts at axon terminals of turtle photoreceptors: difference in sensitivity among cell types.Proceedings of National Academy of Sciences (USA) 81, 7961–4.

    Google Scholar 

  • Takatsu, N., Nakatani, T., Arikuni, T. &Kimura, H. (1987) Immunocytochemical localization of γ-aminobutyric acid in the hypoglossal nucleus of the macaque monkey,Macaca fuscata: a light and electron microscopic study.Journal of Comparative Neurology 263, 42–53.

    Google Scholar 

  • Wässle, H. &Chun, M. H. (1989) GABA-like immunoreactivity in the cat retina: light microscopy.Journal of Comparative Neurology 279, 43–54.

    Google Scholar 

  • Yazulla, S. (1986) GABAergic mechanisms in the retina.Progress in Retinal Research 5, 1–52.

    Google Scholar 

  • Yazulla, S. &Brecha, N. (1981) Localized binding of [3H]muscimol to synapses in chicken retina.Proceeding of National Academy of Sciences (USA) 78, 643–7.

    Google Scholar 

  • Yazulla, S., Studholme, K. M., Victorica, V. &DeBlas, A. L. (1989) Immunocytochemical localization of GABAA receptors in goldfish and chicken retinas.Journal of Comparative Neurology 280, 15–26.

    Google Scholar 

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Araki, M., Kimura, H. GABA-like immunoreactivity in the developing chick retina: differentiation of GABAergic horizontal cell and its possible contacts with photoreceptors. J Neurocytol 20, 345–355 (1991). https://doi.org/10.1007/BF01355531

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  • DOI: https://doi.org/10.1007/BF01355531

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