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The role of GABA during development of the outer retina in the rabbit

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Abstract

Horizontal cells are among the first to mature in the neonatal mammalian retina and they are the first to establish the position of the outer synaptic layer which is subsequently formed by invading terminals of both rod and cone photoreceptors (1–5). During the period of cone synaptogenesis, horizontal cells transiently express the full complement of GABAergic properties (uptake, release, synthesis and storage of GABA); later during development of rod terminals, these properties are down-regulated (1,6–9_. Given the reports of GABA's role in other developing neuronal systems (for review: 10), we have examined the effect that GABA, produced from horizontal cells, might have on photoreceptor maturation in rabbit retina. Results from our previous studies show that lesioning the horizontal cell with kainic acid in vivo leads to a displacement of cone photoreceptor cells and a disappearance of their synaptic terminals, while rod cells maintain their normal position and produce an overabundance of terminals (11). Similar effects are seen with the GABA-A receptor antagonists, picrotoxin and bicucculine (11,12). New evidence from3H-thymidine studies suggests that the effects of kainic acid are specific and that cell division, migration and differentiation in other cell types do not appear to be affected. This body of work is summarized and possible mechanisms of action are suggested which could account for the apparent ability of GABA to help maintain the normal position of cone cell bodies and regulate cone synaptogenesis.

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References

  1. Schnitzer, M., and Rusoff, A. C. 1984. Horizontal cells of the mouse retina contain glutamic acid decarboxylase-like immunoreactivity during early developmental stages. J. Neurosci. 4:2948–2955.

    Google Scholar 

  2. Stone, J., Egan, M., and Rapapport, D. H. 1985. The site of commencement of retinal maturation in the rabbit. Vis. Res. 25:309–317.

    Google Scholar 

  3. Zimmerman, R. P., Polley, E., and Fortney, R. L. 1988. Cell birthdays and rate of differentiation of ganglion and horizontal cells in the developing cat's retina. J. Comp. Neurol. 274:77–90.

    Google Scholar 

  4. Polley, E. H., Zimmerman, R. P., and Fortney, R. L. 1989. Neurogenesis and maturation of cell morphology in the development of the mammal. Pages 3–39,in Finlay, B. L. and Sengelaub, D. R. (eds.) Development of the Vertebrate Retina, Pergamon Press, New York.

    Google Scholar 

  5. Redburn, D. A. 1992. Development of GABAergic neurons in the mammalian retina. Pages 133–147,in Mize, R. R., Marc, R. R. and Sillito, A. M. (eds.) Progress in Brain Research, Vol. 90, Elsevier, New York.

    Google Scholar 

  6. Brandon, C., Lam, D. M. L., and Wu, J. Y. 1979. The gamma aminobutyric acid system in rabbit retina: Localization by immunocytochemistry and autoradiography. Proc. Natl. Acad. Sci. USA 76:3557–3561.

    Google Scholar 

  7. Redburn, D. A., and Madtes, P. 1986. Postnatal development of3H-GABA accumulating cells in rabbit retina. J. Comp. Neurol. 243:41–57.

    Google Scholar 

  8. Redburn, D. A., and Keith, M. E. 1987. Developmental alterations in retinal GABAergic neurons. Pages 79–108,in Neurotrophic Activity of GABA During Development, Redburn, D. A., and Schousboe, A., (eds.) Alan R. Liss, New York.

    Google Scholar 

  9. Messersmith, E. K., and Redburn, D. A. 1992. Gamma aminobutyric acid immunoreactivity in multiple cell types of the developing rabbit retina. Vis. Neurosci. 8:201–211.

    Google Scholar 

  10. Redburn, D. A. and Schousboe, A. (eds.) 1987. Neurotrophic Activity of GABA During Development Alan R. Liss, New York.

    Google Scholar 

  11. Messersmith, E. K., and Redburn, D. A. 1990. Kainic acid lesioning alters outer plexiform layer development in neonatal rabbit retina. Inter. J. Dev. Neurosci. 8:447–461.

    Google Scholar 

  12. Messersmith, E. K., and Redburn, D. A. 1992. Blocking the GABA-A receptor alters cone photoreceptor differentiation. In preparation.

  13. Ghosh, A., Antonin, A., McConnell, S. K., and Shatz, C. J. 1990. Requirement for subplate neurons in the formation of thalamocortical connections. Nature 347:179–181.

    Google Scholar 

  14. Osborne, N. N., Patel, S., Beaton, D. W., and Neuhoff, V. 1986. GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell Tiss. Res. 243:117–123.

    Google Scholar 

  15. 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 

  16. Chronwall, B. M. and Wolff, J. R. 1980. Prenatal and postnatal development of GABA-accumulating cells in the occipital neocortex of rat. J. Comp. Neurol. 190:187–208.

    Google Scholar 

  17. Madtes, P. Jr., and Redburn, D. A. 1983. GABA as a trophic factor during development. Life Sci. 33:979–984.

    Google Scholar 

  18. Meier, E., Drejer, J., and Schousboe, A. 1983. Trophic actions of GABA on the development of physiologically active GABA receptors. Psychopharmacol. Vol. 37, Pages 47–58,in Mandel, P. and DeFeudis, F. V. (eds.), CNS-Receptors from Molecular Pharmacology to Behavior, Raven Press, New York.

    Google Scholar 

  19. Hansen, G. H., Meier, E., and Schousboe, A. 1984. GABA influences the ultrastructure composition of cerebellar granule cells during development in culture. Int. J. Devel. Neurosci. 2:247–257.

    Google Scholar 

  20. Gordon-Weeks, P. R., Lockerbie, R. O., and Pearce, B. R. 1984. Optake and release of [3H]GABA by growth cones isolated from neonatal rat brain. Neurosci. Lett. 52:205–210.

    Google Scholar 

  21. Lockerbie, R. O. and Gordon-Weeks, P. R. 1985. Gamma aminobutyric acid (GABA) receptors modulate [3H]GABA release from isolated neuronal growth cones in the rat. Neurosci. Lett. 55:273–277.

    Google Scholar 

  22. Lockerbie, R. O., Gordon-Weeks, P. R., and Pearce, B. R. 1985. Growth cones isolated from developing rat forebrain: Uptake and release of GABA and noradrenaline. Develop. Brain Res. 20:176–180.

    Google Scholar 

  23. Carter-Dawson, L. D. and LaVail, M. M. 1979. Rods and cones in the mouse retina. II. Autoradiographic analysis of cell generation using tritated thymidine. J. Comp. Neurol. 188:263–272.

    Google Scholar 

  24. Hinds, J. W. and Hinds, P. L. 1979. Differentiation of photoreceptors and horizontal cells in the embryonic mouse retina: An electron microscopic, serial section analysis. J. Comp. Neurol. 187:495–512.

    Google Scholar 

  25. Maslim, J. and Stone, J. 1986. Synaptogenesis in the retina of the cat. Brain Res. 373:35–48.

    Google Scholar 

  26. Sidman, R. L. 1961. Histogenesis of mouse retina studied with3H-thymidine. Pages 487–492,in Smelser, G. K. (ed) Structure of the Eye, Academic Press, New York.

    Google Scholar 

  27. Moran, J., Pasantes-Morales, H. and Redburn, D. A. 1986. Glutamate receptor agonists release3H-GABA preferentially from horizontal cells. Brain Res. 398:276–287.

    Google Scholar 

  28. Redburn, D. A., Agarwal, S. A., Messersmith, E. K., and Mitchell, C. K. 1992. Development of the glutamate system in rabbit retina. Neurochem. Res. 17:61–66.

    Google Scholar 

  29. Blanks, J. C. and Johnson, L. V. 1984. Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison. Invest. Ophthalmol. Vis. Sci. 25:546–557.

    Google Scholar 

  30. Wikler, K. C. and Rakic, P. 1991. Relation of an array of early differentiating cones to the photoreceptor mosaic in the primate retina. Nature 351:391–400.

    Google Scholar 

  31. Forscher, P. 1989. Calcium and polyphosphoinositide control of cytoskeletal dynamics. Trends Neurosci. 12:468–474.

    Google Scholar 

  32. Anglister, L., Farber, I. C., Sharar, C. A., Ginvald, A. 1982. Location of voltage sensitive calcium channels along developing neurites: their possible role in regulation of neurite elongation. Dev. Biol. 94:351–365.

    Google Scholar 

  33. Bolsover, S. R. and Spector, I. 1986. Measurements of calcium transients in the somas, neurite and growth cone of single cultured neurons. J. Neurosci. 6:1934–1940.

    Google Scholar 

  34. Cohan, C. S., Connor, J. A., and Kater, S. B. 1987. Electrically and chemically mediated increases in intracellular calcium in neuronal growth cones. J. Neurosci. 7:3588–3599.

    Google Scholar 

  35. Lipton, S. A. and Kater, S. B. 1989. Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci. 12:265–270.

    Google Scholar 

  36. Bentley, D., Guthrie, P. B. and Kater, S. B. 1991. Calcium ion distribution in nascent pioneer axons and coupled preaxonogenesis neurons in situ. J. Neurosci. 11:1300–1308.

    Google Scholar 

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Authors and Affiliations

  1. Department of Neurobiology and Anatomy, The University of Texas Medical School, P.O. Box 20709, 77030, Houston, TX

    Elizabeth K. Messersmith & Dianna A. Redburn Ph.D.

  2. Department of Molecular and Cell Biology, University of California, 94720, Berkeley, CA

    Elizabeth K. Messersmith

Authors
  1. Elizabeth K. Messersmith
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  2. Dianna A. Redburn Ph.D.
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Special issue dedicated to Dr. Claude Baxter

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Messersmith, E.K., Redburn, D.A. The role of GABA during development of the outer retina in the rabbit. Neurochem Res 18, 463–470 (1993). https://doi.org/10.1007/BF00967250

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