Journal of Neurocytology

, Volume 15, Issue 5, pp 645–655 | Cite as

Electron microscopy of glutamate decarboxylase (GAD) immunoreactivity in the inner plexiform layer of the rhesus monkey retina

  • Andrew P. Mariani
  • Maria T. Caserta


With indirect immunofluorescence, glutamate decarboxylase (GAD), the GABA synthesizing enzyme, was localized to cell bodies in the inner half of the inner nuclear layer and a few in the outer tier of the ganglion cell layer in the rhesus monkey retina. In the inner plexiform layer there were three strongly GAD-immunoreactive laminae separated by two less immunoreactive laminae. Electron microscopy demonstrated that the GAD was contained in amacrine cells and these GAD-immunoreactive amacrines were primarily pre- and postsynaptic to biopolar cell axon terminals. The GAD-containing processes possessed small synaptic vesicles and formed synapses that could be characterized as symmetrical. Large, dense-cored vesicles were often found in the cell bodies and synaptic processes of the GAD-immunoreactive amacrine cells. As the vast majority of the synaptic input and output of the GAD-containing amacrine cells was to and from bipolar cells and the strongest GAD-immunoreactivity correlated with the endings of bipolar cells that connect with a single cone, the functional effects of GABA in the primate retina are likely to be found in the responses of single cone pathways in the inner plexiform layer.


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  1. Allen, R. A. (1969) The retinal bipolar cells and their synapses in the inner plexiform layer. InThe Retina: Morphology, Function and Clinical Characteristics (edited byStraatsma, B. R., Hall, M. O., Allen, R. A. &Crescitelli, F.), pp. 101–43. Los Angeles: University of California Press.Google Scholar
  2. Boycott, B. B. &Dowling, J. E. (1969) Organization of the primate retina: light microscopy.Philosophical Transactions of the Royal Society of London, Series B255, 109–76.Google Scholar
  3. 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
  4. Brandon, C., Lam, D. M. K. &Wu, J. Y. (1979) The gamma-aminobutyric acid system in rabbit retina: localization by immunocytochemistry and autoradiography.Proceedings of the National Academy of Sciences USA 76, 3557–61.Google Scholar
  5. Cajal, S. R. y (1933) La retine des vertebres. InThe Structure of the Retina (translated byThorpe, S. A., &Glickstein, M., 1972). Springfield, Illinois: Charles C. Thomas.Google Scholar
  6. Chan-Palay, V., Nilaver, G., Palay, S. L., Beinfeld, M. C., Zimmerman, E. A., Wu, J. Y. &O'Donohue, T. L. (1981) Chemical heterogeneity in cerebellar Purkinje cells: existence and coexistence of glutamic acid decarboxylase-like and motolin-like immunoreactivities.Proceedings of the National Academy of Sciences USA 78, 7787–91.Google Scholar
  7. Coons, A. H. (1958) Fluorescent antibody methods. InGeneral Cytochemical Methods (edited byDanielli, J. F.), pp. 399–422. New York: Academic Press.Google Scholar
  8. Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study.Brain Research 9, 268–87.Google Scholar
  9. Dowling, J. E. &Boycott, B. B. (1966) Organization of the primate retina: electron microscopy.Proceedings of the Royal Society of London, Series B 166, 80–111.Google Scholar
  10. Ehinger, B. (1970) Autoradiographic identification of rabbit retinal neurons that take up GABA.Experientia 26, 1063–4.Google Scholar
  11. Famiglietti, E. V. Jr &Kolb, H. (1975) A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina.Brain Research 84, 293–300.Google Scholar
  12. Gilok, H. &Sedat, J. W. (1982) Fluorescence microscopy: reduced photobleaching of rhodamine and fluorecein in protein conjugates by n-propyl gallate.Science 217, 1252–5.Google Scholar
  13. Gray, E. G. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study.Journal of Anatomy 93, 420–33.Google Scholar
  14. Hendrickson, A., Ryan, M., Noble, B. &Wu, J. Y. (1985) Colocalization of3(H)muscimol and antisera to GABA and glutamic acid decarboxylase within the same neurons in monkey retina.Brain Research 348, 391–6.Google Scholar
  15. Kosaka, T., Hataguchi, Y., Hama, K., Nagatsu, I. &Wu, J. Y. (1985) Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gammaaminobutyric acid (GABA) and dopamine.Brain Research 343, 166–71.Google Scholar
  16. Mariani, A. P. (1981) A diffuse invaginating cone bipolar cell in primate retina.Journal of Comparative Neurology 197, 661–71.Google Scholar
  17. Mariani, A. P. (1982a) ‘Association’ amacrine cells could mediate directional selectivity in pigeon retina.Nature 298, 654–5.Google Scholar
  18. Mariani, A. P. (1982b) Biplexiform cells: ganglion cells of the primate retina that contact photoreceptors.Science 216, 1134–6.Google Scholar
  19. Mariani, A. P. (1983a) A morphological basis for verticality detectors in the pigeon retina: asymmetric amacrine cells.Naturwissenschaften 70, 368–9.Google Scholar
  20. Mariani, A. P. (1983b) Giant bistratified bipolar cells in monkey retina.Anatomical Record 206, 215–20.Google Scholar
  21. Mariani, A. P. (1984a) Bipolar cells in monkey retina selective for the cones likely to be blue sensitive.Nature 308, 185–6.Google Scholar
  22. Mariani, A. P. (1984b) The neuronal organization of the outer plexiform layer of the primate retina.International Review of Cytology 86, 285–320.Google Scholar
  23. Mariani, A. P., Kolb, H. &Nelson, R. (1984) Dopamine-containing amacrine cells of rhesus monkey retina parallel rods in spatial distribution.Brain Research 322, 1–7.Google Scholar
  24. Mosinger, J. L. &Yazulla, S. (1985) Colocalization of GAD-like immunoreactivity and3H-GABA uptake in amacrine cells of rabbit retina.Journal of Comparative Neurology 240, 396–406.Google Scholar
  25. Nelson, R. (1982) AII amacrine cells quicken time course of rod signals in the cat retina.Journal of Neurophysiology 47, 928–47.Google Scholar
  26. Nishimura, Y., Schwartz, M. L. &Rakic, P. (1985) Localization of γ-aminobutyric acid and glutamic acid decarboxylase in rhesus monkey retina.Brain Research 359, 351–5.Google Scholar
  27. Ohara, P. T., Lieberman, A. R., Hunt, S. P. &Wu, J.Y. (1983) Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat.Neuroscience 8, 189–211.Google Scholar
  28. Oertel, W. H., Graybiel, A. M., Mugnaini, E., Elde, R. P., Schmechel, D. E. &Kopin, I. J. (1983) Coexistence of glutamic acid decarboxylase- and somatostatin-like immunoreactivity in neurons of the feline nucleus reticularis thalami.Journal of Neuroscience 3, 1322–32.Google Scholar
  29. Oertel, W. H., Schmechel, D. E., Mugnaini, E., Tappaz, M. L. &Kopin, I. J. (1981) Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum.Neuroscience 6, 2715–35.Google Scholar
  30. Polyak, S. L. (1957) Structure of the retina. InThe Vertebrate Visual System, pp. 207–87. Chicago: University of Chicago Press.Google Scholar
  31. Pourcho, R. G. (1980) Uptake of (2H)glycine and (3H)GABA by amacrine cells in the cat retina.Brain Research 198, 333–46.Google Scholar
  32. Sternberger, L. (1979)Immunocytochemistry. New York: Wiley.Google Scholar
  33. Vallerga, S. &Deplano, S. (1984) Differentiation, extent and layering of amacrine cell dendrites in the retina of a sparid fish.Proceedings of the Royal Society of London, Series B221, 465–77.Google Scholar
  34. Vaney, D. I. (1985) The morphology and topographic distribution of All amacrine cells in the cat retina.Proceedings of the Royal Society of London, Series B224, 475–88.Google Scholar
  35. Vaughn, J. E., Famiglietti, E. V. Jr, Barber, R. P., Saito, K., Roberts, E. &Ribak, C. E. (1981) GABAergic amacrine cells in rat retina: immunocytochemical identification and synaptic connectivity.Journal of Comparative Neurology 197, 113–27.Google Scholar
  36. Venable, J. H. &Coggeshall, R. (1965) A simplified lead citrate stain for use in electron microscopy.Journal of Cell Biology 25, 407–8.Google Scholar
  37. Wong-Riley, M. T. T. (1974) Synaptic organization of the inner plexiform layer in the retina of the tiger salamander.Journal of Neurocytology 3, 1–33.Google Scholar
  38. Wood, J. G., McLaughlin, B. J. &Vaughn, J. E. (1976) Immunocytochemical localization of GAD in electron microscopic preparations of rodent CNS. InGABA in Nervous System Function (edited byRoberts, E., Chase, T. N. &Tower, D. B.), pp. 133–48. New York: Raven Press.Google Scholar
  39. Zucker, C., Yazulla, S. &Wu, J. Y. (1984) Noncorrespondence of (3H)GABA uptake and GAD localization in goldfish amacrine cells.Brain Research 298, 154–8.Google Scholar

Copyright information

© Chapman and Hall Ltd. 1986

Authors and Affiliations

  • Andrew P. Mariani
    • 1
  • Maria T. Caserta
    • 1
  1. 1.Laboratory of Neurophysiology, National Institute of Neurological and Communicative Disorders and StrokeNational Institutes of HealthBethesdaUSA

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