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γ-Aminobutyric acid immunoreactivity in multiple cell types of the developing rabbit retina

Published online by Cambridge University Press:  02 June 2009

Elizabeth K. Messersmith  and
Dianna A. Redburn
Elizabeth K. Messersmith
Affiliation:
Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston
Dianna A. Redburn
Affiliation:
Department of Neurobiology and Anatomy, The University of Texas Medical School at Houston
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Abstract

We have previously demonstrated that the neonatal rabbit retina contains a larger complement of cells that accumulate [3H]-GABA than does the adult. In order for these neurons to be classified as GABAergic, they must also contain endogenous GABA. We now report that these same neonatal cell populations are also immunoreactive to GABA antisera. In frozen sections from rabbit retina, treated with GABA antisera, immunoreactive processes in both synaptic layers were observed at postnatal day 1. The appearance of immunofluorescent fibers precedes that of photoreceptor and bipolar cell terminals in the outer plexiform layer and is diminished by postnatal day 5. Also noted, was a 50% decrease in the density of GABA-immunoreactive cell bodies in the inner nuclear and ganglion cell layers, accompanied by an increase in cell volume and a shift toward a more spherical cell shape of the remaining cells. At postnatal day 1 and 3, we also observed immunoreactive cells having the characteristic morphology of interplexiform cells. This cell type sends branches to both the outer and inner plexiform layers, thus a morphological basis for communication between the two developing plexiform layers is present as early as postnatal day 1. Thus, retinas from neonatal rabbits have a larger complement of cells that stain for endogenous GABA than does the adult. These results coupled with our previous studies suggest that GABAergic properties are expressed by a larger number of cell types in the neonate than in the adult and are consistent with the general hypothesis that GABA functions as a trophic agent during development.

Keywords

ImmunohistochemistryTrophic factorHorizontal cellNeonatal developmentGABA
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 3 , March 1992 , pp. 201 - 211
Copyright
Copyright © Cambridge University Press 1992

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References

Agardh, E., Brunn, A., Ehinger, B. & Storm-Mathisen, J. (1986). GABA immunoreactivity in the retina. Investigative Ophthalmology and Visual Science 27, 674–678.Google ScholarPubMed
Agardh, E., Ehinger, B. & Wu, J.Y. (1987a). GABA and GAD-like immunoreactivity in the primate retina. Histochemistry 86, 485–490.CrossRefGoogle ScholarPubMed
Agardh, E., Brunn, A., Ehinger, B., Ekstrom, P., Veen, T. & Wu, J.Y. (1987ft). Gamma-aminobutyric acid- and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates. Journal of Comparative Neurology 258, 622–630.CrossRefGoogle ScholarPubMed
Blanks, J.C., Adinolfi, A.M. & Lolley, R.N. (1974). Synaptosomes in the photoreceptor terminal of the mouse retina. Journal of Comparative Neurology 156, 81–94.CrossRefGoogle Scholar
Blanks, J.C. & Bok, D. (1977). An autoradiographic analysis of postnatal cell proliferation in the normal and degenerative mouse retina. Journal of Comparative Neurology 174, 317–325.CrossRefGoogle ScholarPubMed
Brandon, C., Lam, D.M.K. & Wu, J.Y. (1979). The γ-aminobutyric acid system in rabbit retina: Localization by immunocytochemistry and autoradiography. Proceedings of National Academy of Sciences of the U.S.A. 76, 3557–3561.CrossRefGoogle ScholarPubMed
Brandon, C. (1987). Cholinergic neurons in the rabbit retina: immunocytochemical localization, and relationship to GABAergic and cholinesterase-containing neurons. Brain Research 401, 385–391.CrossRefGoogle ScholarPubMed
Brecha, N., Johnson, D., Peichl, L. & Wassle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and γ-aminobutyrate immunoreactivity. Proceedings of National Academy of Sciences of the U.S.A. 85, 6187–6191.CrossRefGoogle ScholarPubMed
Cajal, S.R. (1883). La retina des vertebras. In The Vertebrate Retina, translated Rodieck, R.W., pp. 777–904. San Francisco, California: W.H. Freeman and Co.Google Scholar
Chronwall, B.M. & Wolff, J.R. (1980). Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat. Journal of Comparative Neurology 190, 187–208.CrossRefGoogle ScholarPubMed
Ehinger, B. (1970). Autoradiographic identification of rabbit retinal neurons that take up GABA. Experimental Basel 26, 1063.CrossRefGoogle ScholarPubMed
Ehinger, B. & Falck, B. (1971). Autoradiography Of Some Suspected Neurotransmitter Substances: Gaba, Glycine, Glutamic Acid, Histamine, Dopamine, And L-Dopa. Brain Research 33, 157–172.CrossRefGoogle ScholarPubMed
Gordon-Weeks, P.R., Lockerbie, R.O. & Pearce, B.R. (1984). Uptake and release of [3H]-GABA, by growth cones isolated from neonatal rat brain. Neuroscience Letters 52, 205–210.CrossRefGoogle ScholarPubMed
Grunert, U. & Wassle, H. (1990). GABA-like immunoreactivity in the macaque monkey retina: A light and electron microscopic study. Journal of Comparative Neurology 297, 509–524.CrossRefGoogle ScholarPubMed
Hansen, G.H., Meier, E., Abraham, J. & Schousboe, A. (1987). Trophic effects of GABA on cerebellar cells in culture. In Neurotrophic Activity of GABA During Development, ed. Redburn, D.A. & Schousboe, A., pp. 109–138, New York: Alan R. Liss.Google Scholar
Hodgson, A.J., Penke, B., Erdei, A., Chubb, L.W. & Somogy, P. (1985). Antisera to γ-aminobutyric acid. I. Production and characterization using a new model system. Journal of Histochemistry and Cytochemistry 33, 229–239.CrossRefGoogle ScholarPubMed
Johns, P., Rusoff, A.C. & Dubin, M.W. (1979). Postnatal neurogenesis in the kitten retina. Journal of Comparative Neurology 187, 545–552.CrossRefGoogle ScholarPubMed
Joo, F., Dames, W. & Wolff, J.R. (1979). Effect of prolonged sodium bromide administration on the fine structure of dendrites in the superior cervical ganglion of adult rat. In Development and Chemical Specificity of Neurons, ed. Cuenod, M., Kreutzberg, G.W. & Blooms, F.E., pp. 109–115. Progress in Brain Research, Vol. 51.CrossRefGoogle Scholar
Koontz, M.A. & Hendrickson, A.E. (1990). Distribution of GABA-immunoreactive amacrine cell synapses in the inner plexiform layer of macaque monkey retina. Visual Neuroscience 5, 17–28.CrossRefGoogle ScholarPubMed
Lockerbie, R.O. & Gordon-Weeks, P.R. (1985). γ-aminobutyric acid (GABA) receptors modulate [3H]-GABA release from isolated neuronal growth cones in the rat. Neuroscience Letters 55, 273–277.CrossRefGoogle ScholarPubMed
Lockerbie, R.O., Gordon-Weeks, P.R. & Pearce, B.R. (1985). Growth cones isolated from developing rat forebrain: Uptake and release of GABA and noradrenaline. Developmental Brain Research 20, 176–180.Google Scholar
MadtesP., Jr P., Jr & Redburn, D.A. (1983). GABA as a trophic factor during development. Life Sciences 33, 979–984.CrossRefGoogle ScholarPubMed
Marshburn, P.B. & Luvone, P.M. (1981). The role of GABA in the regulation of the dopamine tyrosine hydroxylase-containing neurons of the rat retina. Brain Research 214, 335–347.CrossRefGoogle ScholarPubMed
Maslim, J. & Stone, J. (1986). Synaptogenesis in the retina of the cat. Brain Research 373, 35–48.CrossRefGoogle ScholarPubMed
Massey, S.C. & Redburn, D.A. (1982). A tonic GABA-mediated inhibition of cholinergic amacrine cells in rabbit retina. Journal of Neuroscience 2, 1633–1643.CrossRefGoogle Scholar
McArdle, C.B., Dowling, J.E. & Masland, R.H. (1977). Development of outer segments and synapses in the rabbit retina. Journal of Comparative Neurology 175, 253–274.CrossRefGoogle ScholarPubMed
Messersmith, E.K. & Redburn, D.A. (1990). Differentiation of retinal cell types after kanic acid treatment. Journal of Cell Biology 109, 239a.Google Scholar
Miller, R.F. & Dacheaux, R.F. (1975). Chloride sensitive receptive field mechanism in the isolated retina eye-cups of the rabbit retina. Brain Research 90, 329–334.CrossRefGoogle Scholar
Mosinger, J.L. & Yazulla, S. (1985). Colocalization of GAD-like immunoreactivity and [3H]-GABA uptake in amacrine cells of rabbit retina. Journal of Comparative Neurology 240, 396–406.CrossRefGoogle ScholarPubMed
Mosinger, J. & Yazulla, S. (1987). Double-label analysis of GAD- and GABA-like immunoreactivity in the rabbit retina. Vision Research 27, 23–30.CrossRefGoogle ScholarPubMed
Mosinger, J., Yazulla, S. & Studholme, K.M. (1986). GABA-like immunoreactivity in the vertebrate retina: A species comparison. Experimental Eye Research 42, 631–644.CrossRefGoogle ScholarPubMed
Nakamura, Y., McGuire, B.A. & Sterling, P. (1980). Interplexiform cells in the cat retina: Identification by uptake of [3H]γ-aminobutyric acid and serial reconstruction. Proceedings of National Academy of Sciences of the U.S.A. 77, 658–661.CrossRefGoogle ScholarPubMed
Nishimura, Y., Schwartz, M.L. & Rakic, P. (1985). Localization of γ-aminobutyric acid and glutamic acid decarboxylase in rhesus monkey. Brain Research 359, 351–355.CrossRefGoogle ScholarPubMed
Osborne, N.N., Patel, S., Beaton, D.W. & Neuhoff, V. (1986). GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell Tissue Research 243, 117–123.CrossRefGoogle ScholarPubMed
Oyster, C.W. & Takahashi, E.S. (1977). Interplexiform cells in rabbit retina. Proceedings of the Royal Society B (London) 197, 477–484.Google ScholarPubMed
Polley, E.H., Zimmerman, R.P. & Fortney, R.L. (1985). Development of the outer plexiform layer (OPL) of the cat retina. Society of Neuroscience Abstracts 11, 14.Google Scholar
Pourcho, R.G. & Owczarzak, M.T. (1989). Distribution of GABA immunoreactivity in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 2, 425–435.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Goebel, D.J. (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist, [3H]-muscimol: A combined Golgi and autoradiographic study. Journal of Comparative Neurology 219, 24–35.Google ScholarPubMed
Redburn, D.A. & Madtes, P. Jr (1986). Postnatal development of [3H]-GABA accumulating cells in rabbit retina. Journal of Comparative Neurology 243, 41–57.CrossRefGoogle ScholarPubMed
Ryan, M.K. & Hendrickson, A.E. (1987). Interplexiform cells in macaque monkey retina. Experimental Eye Research 45, 57–66.CrossRefGoogle ScholarPubMed
Schnitzer, M. & Rusoff, A.C. (1984). Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. Journal of Neuroscience 4, 2948–2955.CrossRefGoogle ScholarPubMed
Sidman, R.L. (1961). Histogenesis of mouse retina studied with [3H]-thymidine. In Structure of the Eye, ed. Smelser, G.K., pp. 487–492, New York: Academic Press.Google Scholar
Sidman, R.L. (1986). Histogenesis of mouse retina studied with [3H]-thymidine. In Structure of the Eye, ed. Smelser, G.K., pp. 487–492. Academic Press.Google Scholar
Spoerri, P.E. & Wolff, J.R. (1982). Morphological changes induced by sodium bromide in murine neuroblastoma cells in vitro. Cell Tissue Research 222, 379–388.CrossRefGoogle ScholarPubMed
Wassle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 43–54.CrossRefGoogle ScholarPubMed
Wolff, J.R. (1979). Indication for a dual role of GABA as a synaptic transmitter and as a morphogenetic factor. Verh. dt. zool. Ges 197, 194–200.Google Scholar
Wolff, J.R., Richman, M. & Chronwall, B.M. (1979a). Axo-glial synapses and GABA-accumulating glial cells in the embryonic neocortex of the rat. Cell Tissue Research 201, 239–248.CrossRefGoogle ScholarPubMed
Wolff, J.R., Joo, F., Dames, W. & Feher, O. (1979b). Induction and maintenance of free postsynaptic membrane thickening in the adult superior cervical ganglion. Journal of Neurocytology 8, 549–563.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, Vol. 5, ed. Osborne, N. & Chader, G., pp. 1–52. Oxford: Pergamon Press.Google Scholar
Yu, B.C.W., Wyatt, C.B., Lam, D.M.K. & Fry, K.R. (1987a). GABAergic ganglion cells in the rabbit retina. Investigative Ophthalmology and Visual Science (Suppl.) 28, 349.Google Scholar
Yu, B.C.W., Watt, C.B., Lam, D.M.K. & Fry, K.R. (1987b). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376–382.CrossRefGoogle Scholar