Skip to main content
    • Aa
    • Aa

GABAA receptors in the retina of the cat: An immunohistochemical study of wholemounts, sections, and dissociated cells

  • Thomas E. Hughes (a1) (a2), Ulrike Grönert (a2) and Harvey J. Karten (a1)

Gamma-aminobutyric acid (GABA) is an inhibitory neurotransmitter used by many neurons of the mammalian retina. To identify the synaptic targets of these cells, we undertook an immunohistochemical study with a monoclonal antibody that recognizes the GABAA receptors (62−3G1, generously donated by A. de Blas). This antibody labels the somata of at least one group of amacrine cells in the inner nuclear layer. It also labels two groups of somata in the ganglion cell layer: one small and the other much larger. The small cells are likely to be displaced amacrine cells based on their size, although some could be gamma ganglion cells. The much larger receptor-positive cells are clearly ganglion cells, based both on their size and the antibody labeling of the initial portion of their axon. In the peripheral retina, the size of these large somata suggests that many are beta ganglion cells. However, at any point across the retina the density of these cells never exceeded 50% of the density of beta cells as a whole.

The antibody also labels a dense plexus of processes that extends throughout the inner plexiform layer (IPL), with a marked concentration in the inner third of the layer. This is the portion of the IPL in which the rod bipolar cells terminate. It is difficult to recognize processes of individual cells in the IPL, so retinae were dissociated. The rod bipolar cells were identified by protein kinase C immunoreactivity (Negishi et al., 1988; Karschin & Wässle, 1990). They were not labeled by the GABAA receptor antibody. This is surprising in light of tight-seal, whole cell voltage-clamp recordings that have shown that the rod bipolars express functional GABAA receptors. One possible explanation is that the antibody recognizes only a subset of the GABAA receptors.

Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

R.A. Altschuler , H. Betz , M.H. Parakkal , K.A. Reeks & R.J. Wenthold (1986). Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor. Brain Research 369, 316320.

E.A. Barnard , M.G. Darlison & P. Seeburg (1987). Molecular biology of the GABAA receptor: the receptor/;channel superfamily. Trends in Neuroscience 10, 502509.

J. Bolz , T. Frumkes , T. Voigt & H. Wässle (1985). Action and localization of gamma-aminobutyric acid in the cat retina. Journal of Physiology (London) 362, 369393.

B.B. Boycott & H. Wässle (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397419.

N. Brecha , A. Francis & N. Schechter (1971). Rapid loss of nicotine-cholinergic receptor binding activity in the deafferented avian optic lobe. Brain Research 167, 273280.

M.H. Chun & H. Wässle (1989). GABA-like immunoreactivity in the cat retina: electron miscroscopy. Journal of Comparative Neurology 279, 5567.

M.A. Freed , R.G. Smith & P. Sterling (1987). Rod bipolar array in the cat retina: pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445455.

G. Greeningloh , A. Rienitz , B. Schmitt , C. Methfessel , M. Zensen , K. Beyreuther , E.D. Gundelfinger & H. Betz (1987). The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors. Nature 328, 215220.

U. Greferath , U. Grönert & H. Wässle (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433442.

P. Häring , C. Stahli , P. Schoch , B. Takacs , T. Staehelin & H. Möhler (1985). Monoclonal antibodies reveal structural homogeneity of gamma-aminobutyric acid/;benzodiazepine receptor in different brain areas. Proceedings of the National Academy of Sciences of the U.S.A. 82, 48374841.

J.M. Henley , J.M. Lindstrom & R.E. Oswald (1986). Acetylcholine receptor synthesis in retina and transport to optic tectum in goldfish. Science 232, 16271629.

R. Huba & H-D. Hofmann (1988). Tetanus toxin binding to isolated and cultured rat retinal glial cells. Glia 1, 156164.

J.M. Juiz , R.H. Helfert , R.J. Wenthold , A.L. De Blas & R.A. Altschuler (1989). Immunocytochemical localization of the GABAA receptor/;benzodiazepine receptor in the guinea pig cochlear nucleus: evidence for receptor localization heterogeneity. Brain Research 504(1), 173179.

A. Kaneko & M. Tachibana (1986). Effects of gamma-aminobutyric acid on isolated cone photoreceptors of the turtle retina. Journal of Physiology (London) 373, 443461.

K. Keinänen , W. Wisden , B. Sommer , P. Werner , A. Herb , T.A. Verdoorn , B. Sakmann & P.H. Seeburg (1990). A family of AMPA-selective glutamate receptors. Science 249, 556560.

H. Kolb & R. Nelson (1983). Rod pathways in the retina of the cat. Vision Research 23, 301–12.

H. Kolb , R. Nelson & A. Mariani (1981). Amacrine cells, bipolar cells, and ganglion cells of the cat retina: a Golgi study. Vision Research 21, 10181114.

E.S. Levitan , L.A.C. Blair , V.E. Dionne & E.A. Barnard (1988). Biophysical and pharmacological properties of cloned GABAA receptor subunits expressed in Xenopus oocytes. Neuron 1, 773781.

A.P. Mariani , D. Cosenza-Murphy & J.L. Barker (1987). GABAergic synapses and benzodiazepine receptors are not identically distributed in the primate retina. Brain Research 415, 152157.

J.L. Mosinger , S. Yazulla & K.M. Studholme (1986). GABA-like immunoreactivity in the vertebrate retina: a species comparison. Experimental Eye Research 42, 631644.

Y. Nakamura , B.A. McGuire & P. Sterling (1980). Interplexiform cell in cat retina: identification by uptake of [3H]GABA and serial reconstruction. Proceedings of the National Academy of Sciences of the U.S.A. 77, 658661.

K. Negishi , S. Kato & T. Teranishi (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247252.

W.H. Oertel , D.E. Schmechel , M.A. Tappaz & I.J. Kopin (1981). Production of a specific antiserum to rat brain glutamic-acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6, 26892700.

R.G. Pourcho (1980). Uptake of [3H]-glycine and [3H]-GABA by amacrine cells in the cat retina. Brain Research 198, 333346.

R.G. Pourcho (1981). Autoradiographic localization of [3H]- muscimol in the cat retina. Brain Research 215, 187199.

R.G. Pourcho & D.J. Goebel (1983). Neuronal subpopulations in cat retina which accumulate the GABA agonist, [3H]-muscimol: a combined Golgi and autoradiographic study. Journal of Comparative Neurology 219, 2535.

D.B. Pritchett , H. Sontheimer , B.D. Shivers , S. Ymer , H. Kettenmann , P.R. Schofield & P.H. Seeburg (1989). Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature 338, 582.

P.V. Sarthy & D.M.-K. Lam (1979). Isolated cells from a mammalian retina. Brain Research 176, 208212.

P.V. Sarthy & M. Fu (1989). Localization of L-glutamic acid decarboxylase mRNA in cat retinal horizontal cells by in situ hybridization. Journal of Comparative Neurology 288, 593600.

P. Schoch , P. Häring , B. Takacs , C. Stähli & H. Möhler (1984). A GABA/;benzodiazepine receptor complex from bovine brain: Purification, reconstitution and immunological characterization. Journal of Receptor Research 4, 189200.

I. Soltesz , J.D.B. Roberts , H. Takagi , J.G. Richards , H. Mohler & P. Somogyi (1990). Synaptic and nonsynaptic localization of benzodiazepine/;GABAA receptor/;Cl-channel complex using monoclonal antibodies in the dorsal lateral geniculate nucleus of the cat. European Journal of Neuroscience 2, 414429.

R.A. Stephenson , S.O. Casalotti , C. Mamalaki & E.A. Barnard (1986). Antibodies recognizing the GABAA/;benzodiazepine receptor included its regulatory sites. Journal of Neurochemistry 46, 854861.

J.K. Stevens , B.A. McGuire & P. Sterling (1980). Toward a functional architecture of the retina: serial reconstruction of adjacent ganglion cells. Science 207, 317319.

J. Strom-Mathisen , A.K. Liknes , A.T. Bore , J.L. Vaaland , P. Edminson , M.S. Haug & O.P. Ottersen (1983). First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301, 517520.

S. Suzuki , M. Tachibana & A. Kaneko (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology (London) 421, 645662.

M. Tachibana & A. Kaneko (1987). Gamma-aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells: evidence for negative feedback from amacrine cells. Proceedings of the National Academy of Sciences of the U.S.A. 84, 35013505.

A. Triller , F. Cluzeaud , F. Pfeiffer , H. Betz & H. Korn (1985). Distribution of glycine receptors at central synapses: an immunoelectron microscopy study. Journal of Cell Biology 101, 683688.

D. Vaney (1990). The mosaic of amacrine cells in the mammalian retina. In Progress in Retinal Research, Vol. 9, ed. N.N. Osborne & G.J. Chader , pp. 49100. Oxford:Pergamon Press.

H. Wässle (1982). Morphological types and central projections of ganglion cells in the cat retina. In Progress in Retinal Research, Vol. 1, ed. N.N. Osborne & G.J. Chader , pp. 125152. Oxford: Pergamon Press.

H. Wässle & M.H. Chun (1989). GABA-like immunoreactivity in the cat retina: light microscopy. Journal of Comparative Neurology 279, 4354.

H. Wässle , W.R. Levick & B.G. Cleland (1975). The distribution of the alpha type of ganglion cells in the cat's retina. Journal of Comparative Neurology 159(3), 419438.

H. Wässle , M.H. Chun & F. Müller (1987). Amacrine cells in the ganglion cell layer of the cat retina. Journal of Comparative Neurology 265, 391408.

R.J. Wenthold , M.H. Parakkal , M.D. Oberdorfer & R.A. Altschuler (1988). Glycine receptor immunoreactivity in the ventral cochlear nucleus of the guinea pig. Journal of Comparative Neurology 276, 423435.

W. Wisden , B.J. Morris , M.G. Darlison , S.P. Hunt & E.A. Barnard (1988). Distinct GABAAA receptor α subunit mRNAs show different patterns of expression in bovine brain. Neuron 1, 937947.

R.O.L. Wong & A. Hughes (1987). The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina. Journal of Comparative Neurology 255, 159177.

S. Yazulla , K.M. Studholme , J. Vitorica & A.L. de Blas (1989). Immunocytochemical localization of GABAA receptors in goldfish and chicken retinas. Journal of Comparative Neurology 280, 1526.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Visual Neuroscience
  • ISSN: 0952-5238
  • EISSN: 1469-8714
  • URL: /core/journals/visual-neuroscience
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Full text views

Total number of HTML views: 0
Total number of PDF views: 1 *
Loading metrics...

Abstract views

Total abstract views: 80 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 29th May 2017. This data will be updated every 24 hours.