Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-24T19:47:29.547Z Has data issue: false hasContentIssue false
  • English
  • Français

Horizontal cells in cat and monkey retina express different isoforms of glutamic acid decarboxylase

Published online by Cambridge University Press:  02 June 2009

Noga Vardi ,
Daniel L. Kaufman  and
Peter Sterling
Noga Vardi
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
Daniel L. Kaufman
Affiliation:
Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles
Peter Sterling
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
Get access Rights & Permissions [Opens in a new window]

Abstract

The neurotransmitter used by horizontal cells in mammals has not been identified. GABA has been the leading candidate, but doubt has remained because of failure to clearly demonstrate the GABA synthetic enzyme, glutamic acid decarboxylase (GAD) in these cells. Because GAD was recently shown to exist as two isoforms, 65 kDa and 67 kDa, we considered whether there might be a mismatch between the forms of GAD expressed in horizontal cells and the probes used to detect it. Accordingly, we stained sections of mammalian retina with antibodies specific for each isoform. Cat horizontal cells of both types (A and B) were immunoreactive for GAD67 but negative for GAD65; monkey horizontal cells of both types (H1 and H11) were positive for GAD65 and negative for GAD67. The findings reconcile previous, apparently conflicting, observations and strengthen considerably the hypothesis that mammalian horizontal cells are GABAergic.

Keywords

RetinaCatMonkeyGABAGAD65GAD67Horizontal cellBipolar cells
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 1 , January 1994 , pp. 135 - 142
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agardh, E., Bruun, A., Ehinger, B., Ekstrom, P., van Veen, T. & Wu, J.-Y. (1987a). Gamma-aminobutyric acid- and glutamic acid decarboxylase-immunoreactive neurons in the retina of different vertebrates. Journal of Comparative Neurology 258, 622–630.CrossRefGoogle ScholarPubMed
Agardh, E. & Ehinger, B. (1983). Retinal GABA neuron labelling with (3H) isoguvacine in different species. Experimental Eye Research 36, 215–229.CrossRefGoogle ScholarPubMed
Agardh, E., Ehinger, B. & Wu, J.-Y. (1987 b). GABA and GAD-like immunoreactivity in the primate retina. Histochemistry 86, 485–490.CrossRefGoogle ScholarPubMed
Barlow, H.B. (1961). Three points about lateral inhibition. In Sensory Communication, ed. Rosenblith, W.A., pp. 782–786. Cambridge, Massachusetts: MIT Press.Google Scholar
Bolz, J., Frumkes, T., Voigt, T. & Wässle, H. (1985). Action and localization of gamma-aminobutyric acid in the cat retina. Journal of Physiology 362, 369–393.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Dowling, J.E. (1969). Organization of the primate retina: Light microscopy. Philosophical Transactions of the Royal Society B (London) 255, 109–184.Google Scholar
Boycott, B.B., Peichl, L. & Wässle, H. (1978). Morphological types of horizontal cell in the retina of the domestic cat. Philosophical Transactions of the Royal Society B (London) 203, 229–245.Google ScholarPubMed
Brandon, C. (1985). Retinal GABA neurons: Localization in vertebrate species using an antiserum to rabbit brain glutamate decarboxylase. Brain Research 344, 286–295.CrossRefGoogle ScholarPubMed
Brandon, C., Lam, D.M.K. & Wu, J.-Y. (1979). The gamma-amino butyric acid system in rabbit retina: Localization by immunocyto-chemistry and autoradiography. Proceedings of the National Academy of Sciences of the U.S.A. 76, 3557–3561.CrossRefGoogle Scholar
Brecha, N. (1983). Retinal neurotransmitters: Histochemical and biochemical. In Clinical Neuroanatomy, ed. Emerson, P.C., pp. 85–129. New York: Raven Press.Google Scholar
Brecha, N. (1992). Expression of GABAA receptors in the vertebrate retina. In Progress in Brain Research: GABA in the Retina and in Central Nervous System, Vol. 90, eds. Mize, R.R., Marc, R. & Sillito, A., pp. 3–28. Amsterdam: Elsevier.Google Scholar
Chang, Y.-C. & Gottlieb, D.I. (1988). Characterization of the proteins purified with monoclonal antibodies to glutamic acid decarboxylase. Journal of Neuroscience 8, 2123–2130.CrossRefGoogle ScholarPubMed
Crooks, J. & Kolb, H. (1992). Localization of GABA, glycine, glutamate and tyrosine hydroxylase in the human retina. Journal of Comparative Neurology 315, 287–302.CrossRefGoogle ScholarPubMed
Davanger, S., Ottersen, O.P. & Storm-Mathisen, J. (1991). Glutamate, GABA and glycine in the human retina: An immunocytochemical investigation. Journal of Comparative Neurology 311, 483–494.CrossRefGoogle ScholarPubMed
Erlander, M.G., Tillakarante, N.J.K., Feldblum, S., Patel, N. & Tobin, A.J. (1991). Two genes encode distinct glutamate decarboxylase. Neuron 7, 91–100.CrossRefGoogle Scholar
Freed, M.A. (1992). GABAergic circuits in mammalian retina. In Progress in Brain Research: GABA in the Retina and in the Central Nervous System, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A., pp. 107–132. Amsterdam: Elsevier.Google Scholar
Freed, M.A., Nakamura, Y. & Sterling, P. (1983). Four types of amacrines in the cat retina that accumulate GABA. Journal of Comparative Neurology 219, 295–304.CrossRefGoogle ScholarPubMed
Grünert, U. & Wässle, 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
Hendrickson, A., Ryan, M., Noble, B. & Wu, J.-Y. (1985). Colocalization of (3H)-muscimol and antisera to GABA and glutamic acid decarboxylase within the same neurons in monkey retina. Brain Research 348, 391–395.CrossRefGoogle ScholarPubMed
Hughes, T.E., Carey, R.G., Vitorica, J., de Blas, A.L. & Karten, H.J. (1989). Immunocytochemical localization of GABAA receptors in the retina of the New World primate Saimiri sciureus. Visual Neuroscience 2, 565–581.CrossRefGoogle ScholarPubMed
Kaufman, D.L., Hauser, C.R. & Tobin, A.J. (1991). Two forms of the gamma-aminobutyric acid synthetic enzyme glutamate decar boxylase have distinct intraneuronal distributions and cofactor interactions. Journal of Neurochemistry 56, 720–723.CrossRefGoogle Scholar
Kolb, H. (1970). Organization of the outer plexiform layer of the primate retina: Electron microscopy of Golgi-impregnated cells. Philosophical Transactions of the Royal Society B (London) 258, 261–283.Google ScholarPubMed
Mangel, S.C. (1991). Analysis of the horizontal cell contribution to the receptive field surround of ganglion cells in the rabbit retina. Journal of Physiology 442, 211–234.CrossRefGoogle Scholar
Marc, R.E. (1992). Structural organization of GABAergic circuitry in ectotherm retinas. In Progress in Brain Research: GABA in the Retina and in the Central Nervous System, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A. pp. 61–92. Amsterdam: Elsevier.Google Scholar
Mariani, A.P., Cosenza-Murphy, D. & Barker, J.L. (1987). GABAergic synapses and benzodiazepine receptors are not identically distributed in the primate retina. Brain Research 415, 153–157.CrossRefGoogle Scholar
Masarachia, P., Vardi, N. & Sterling, P. (1991). Localization of GABAA receptor in the outer retina of cat and monkey. Neuroscience Abstracts, #403.7 17, 1013.Google Scholar
Mosinger, J.L. & Yazulla, S. (1987). Double-label analysis of GAD-and GABA-like immunoreactivity in the rabbit retina. Vision Research 27, 23–30.CrossRefGoogle Scholar
Mosinger, J.L., Yazulla, S. & Studholme, K.M. (1986). GABA-like immunoreactivity in the vertebrate retina: A species comparison. Experimental Eye Research 42, 631–644.CrossRefGoogle ScholarPubMed
Nishimura, Y., Schwartz, M.L. & Rakic, P. (1985). Localization of γ-aminobutyric acid and glutamic acid decarboxylase in rhesus monkey retina. Brain Research 359, 351–355.CrossRefGoogle ScholarPubMed
Oertel, W.H., Schmechel, D.E., Tappaz, M.L. & Kopin, I.J. (1981). Production of specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Journal of Neuroscience 6, 2589–2700.Google ScholarPubMed
Pasteels, B., Rogers, J., Blachier, F. & Pochet, R. (1990). Calbindin and calretinin localization in retina from different species. Visual Neuroscience 5, 1–16.CrossRefGoogle ScholarPubMed
Pflug, R., Nelson, R. & Ahnelt, P.K. (1990). Background-induced flicker in cat retinal horizontal cells. I. Temporal and spectral properties. Journal of Neurophysiology 64(2), 313–325.CrossRefGoogle ScholarPubMed
Pourcho, R. (1980). Uptake of (3H)glycine and (3H)GABA by ama-crine cells in the cat retina. Brain Research 198, 333–346.CrossRefGoogle ScholarPubMed
Pourcho, R.G. (1981). Autoradiographic localization of [3H]muscimol in the cat retina. Brain Research 215, 187–199.CrossRefGoogle ScholarPubMed
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
Röhrenbeck, J., Wässle, H. & Boycott, B.B. (1989). Horizontal cells in the monkey retina: Immunocytochemical staining with antibodies against calcium binding proteins. European Journal of Neuroscience 1, 407–420.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Fu, M. (1989 a). Localization of L-glutamic acid decarboxylase mRNA in cat retinal horizontal cells by in situ hybridization. Journal of Comparative Neurology 288, 593–600.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Fu, M. (1989 b). Localization of L-glutamic acid decarboxylase mRNA in monkey and human retina by in situ hybridization. Journal of Comparative Neurology 288, 691–697.CrossRefGoogle ScholarPubMed
Srinivasan, M.V., Laughlin, S.B. & Dubs, A. (1982). Predictive coding: A fresh view of inhibition in the retina. Proceedings of the Royal Society B (London) 216, 427–459.Google ScholarPubMed
Vardi, N., Masarachia, P.J. & Sterling, P. (1992). Immunoreactivity to GABAA receptor in the outer plexiform layer of the cat retina. Journal of Comparative Neurology 320, 394–397.CrossRefGoogle ScholarPubMed
Vaughn, J.E., Famiglietti, E.V., 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, 113–127.CrossRefGoogle ScholarPubMed
Wässle, H. & Chun, M.H. (1989). GABA-like immunoreactivity in the cat retina: Light microscopy. Journal of Comparative Neurology 279, 43–54.CrossRefGoogle ScholarPubMed
Wässle, H., Chun, M.H. & Müller, F. (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 265, 391–408.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. In Progress in Retinal Research, Vol. 5, ed. Osborne, N. & Chader, J., pp. 1–52. Tarrytown, New York: Pergamon Press.Google Scholar