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Distribution of GABA-immunoreactive amacrine cell synapses in the inner plexiform layer of macaque monkey retina

Published online by Cambridge University Press:  02 June 2009

Margaret A. Koontz  and
Anita E. Hendrickson
Margaret A. Koontz
Affiliation:
Department of Ophthalmology, University of Washington School of Medicine, Seattle
Anita E. Hendrickson
Affiliation:
Department of Ophthalmology, University of Washington School of Medicine, Seattle Departments of Biological Structure and Ophthalmology, University of Washington School of Medicine, Seattle
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Abstract

The distribution patterns of GABA immunoreactive (+) and immunonegative (−) amacrine cell synapses and profiles in the inner plexiform layer (IPL) were analyzed in three macaque monkey retinas using postembedding electron-microscopic (EM) immunogold cytochemistry. Synapses and profiles were counted at 5% intervals throughout the IPL depth in three EM montages (total area = 6509 μm2), with 0% depth at the inner nuclear layer/IPL border. Nearly 70% of all amacrine synapses were GABA+, and they contacted all major classes of neurons that arborize in the IPL: bipolars (45%), ganglion cells (25%), and GABA+ (20%) and GABA− (10%) amacrines. A major relationship was seen between GABA+ amacrine processes and bipolar terminals: 76% of all amacrine-to-bipolar synapses were GABA+, and 82% of bipolar output dyads contained at least one GABA+ amacrine.

GABA+ amacrine profiles (N = 2455) were concentrated in three wide bands at IPL depths of 0–25%, 40–60%, and 75–100%, corresponding to the dense bands seen with light-microscopic immunocytochemistry. In contrast, GABA+ amacrine synapses (N = 1081) were distributed evenly throughout the IPL depth, rather than being confined to the three dense bands. GABA− amacrine synapses (N = 516) were concentrated at 40% and 60% depths.

Each category of amacrine output synapses had a characteristic pattern of stratification in the IPL. GABA+amacrine-to-bipolar synapses occurred throughout the IPL but were most frequent at 20% and 80% IPL depths, where the dendrites of midget cone bipolars arborize (Polyak, 1941). In contrast, GABA+amacrine-to-ganglion cell synapses were concentrated at 30% and 70% IPL depths, near the dendritic arborizations of parasol ganglion cells (Watanabe & Rodieck, 1989). GABA+ synapses onto bipolars and amacrines were also concentrated at the level of rod bipolar terminals. GABA+ amacrines must play significant but different roles in ON and OFF midget and parasol pathways as well as the rod pathway.

Keywords

Gamma-aminobutyric acidBipolar cellRetinal ganglion cellVisionImmunocytochemistry
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 1 , July 1990 , pp. 17 - 28
Copyright
Copyright © Cambridge University Press 1990

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References

Agardh, E., Ehinger, B. & Wu, J.-Y. (1987). GABA and GAD-like immunoreactivity in the primate retina. Histochemistry 86, 485–490.CrossRefGoogle ScholarPubMed
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
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
Brecha, N., Hendrickson, A., Floren, I. & Karten, H.J. (1982). Localization of substance P-like immunoreactivity within the monkey retina. Investigative Ophthalmology and Visual Science 23, 147–153.Google ScholarPubMed
Brecha, N., Johnson, D., Peichl, L. & Wässle, H. (1988). Cholinergic amacrine cells of the rabbit retina contain glutamate decarboxylase and gamma-aminobutyrate imrnunoreactivity. Proceedings of the National Academy of Science of the U.S.A. 85, 6187–6191.CrossRefGoogle Scholar
Caruso, D.M., Owczarzak, M.T., Goebel, D.J., Hazlett, J.C. & Pourcho, R.G. (1989). GABA immunoreactivity in ganglion cells of the rat retina. Brain Research 476, 129–135.CrossRefGoogle ScholarPubMed
Chun, M.H. & Wässle, H. (1989). GABA-like immunoreactivity in the cat retina: electron microscopy. Journal of Comparative Neurology 279, 55–67.CrossRefGoogle ScholarPubMed
Chun, M.H.., Wässle, H., & Brecha, N. (1988). Colocalization of [3H]-muscimol uptake and choline acetyltransferase immunoreactivity in amacrine cells of the cat retina. Neuroscience Letters 94, 259–263.CrossRefGoogle ScholarPubMed
Dacheux, R.F. &Raviola, E. (1986). The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Daw, N.W., Brunken, W.J. & Parkinson, D. (1989). The function of synaptic transmitters in the retina. Annual Reviews of Neuroscience 12, 205–225.CrossRefGoogle ScholarPubMed
Dolan, R.P. & Schiller, P.H. (1989). Evidence for only depolarizing rod bipolar cells in the primate retina. Visual Neuroscience 2, 421–424.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: electron microscopy. Proceedings of the Royal Society B (London) 166, 80–111.Google ScholarPubMed
Dowling, J.E., Ehinger, B. & Floren, I. (1980). Fluorescence and electron-microscopical observations on the amine-accumulating neurons of the Cebus monkey retina. Journal of Comparative Neurology 192, 665–685.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr, & Kolb, H. (1976). Structural basis for ON- and OFF-center responses in retinal ganglion cells. Science 194, 193–195.CrossRefGoogle ScholarPubMed
Famiglietti, E.V. Jr, & Vaughn, J.E. (1981). Golgi-impregnated amacrine cells and GABAergic retinal neurons: a comparison of dendritic, immunocytochemical, and histochemical stratification in the inner plexiform layer of rat retina. Journal of Comparative Neurology 197, 129–139.CrossRefGoogle ScholarPubMed
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 2303–2320.CrossRefGoogle ScholarPubMed
Freed, M.A., Smith, R.G. & Streling, P. (1987). Rod bipolar array in the cat retina: pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445–455.CrossRefGoogle ScholarPubMed
Fu, M., Orcutt, J.C. & Sarthy, P.V. (1988). Localization of L-glutamate decarboxylase mRNA in cat and monkey retinas by in situ hybridization. Investigative Ophthalmology and Visual Science (Suppl.) 29, 204.Google Scholar
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, 391–396.CrossRefGoogle ScholarPubMed
Hendrickson, A.E., Koontz, M.A., Pourcho, R.G., Sarthy, P.V. & Goebel, D.J. (1988 a). Localization of glycine-containing neurons in the Macaca monkey retina. Journal of Comparative Neurology 273, 473–487.CrossRefGoogle ScholarPubMed
Hendrickson, A., Mehra, R., Koontz, M. & Tobin, A. (1988 b). Identification of GABAergic neurons in macaque monkey retina. 8th International Congress of Eye Research, San Francisco.Google Scholar
Hokoc, J.N. & Mariani, A.P. (1987). Tyrosine hydroxylase immunoreactivity in the rhesus monkey retina reveals synapses from bipolar cells to dopaminergic amacrine cells. Journal of Neuroscience 7, 2785–2793.CrossRefGoogle ScholarPubMed
Hughes, T.E., Carey, R.G., Vitorica, J., DeBlas, A.L. & Karten, H.J. (1989). Immunohistochemical localization of GABAA receptors in the retina of the New World primate (Saimiri sciureus). Visual Neuroscience 2, 565–582.CrossRefGoogle ScholarPubMed
Kirby, A.W. & Schweitzer-Tong, D.E. (1981). GABA-antagonists and spatial summation in Y-type cat retinal ganglion cells. Journal of Physiology 312, 335–344.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: electron-microscopic observations. Journal of Neurocytology 8, 295–329.CrossRefGoogle ScholarPubMed
Koontz, M.A. & Hendrickson, A.E. (1987). Stratified distribution of synapses in the inner plexiform layer of primate retina. Journal of Comparative Neurology 263, 581–592.CrossRefGoogle ScholarPubMed
Koontz, M.A. & Hendrickson, A.E. (1989). Distribution of GABAergic synapses in the inner retina of macaque monkey. Investigative Ophthalmology and Visual Science (Suppl.) 30, 121.Google Scholar
Koontz, M.A., Hendrickson, A.E. & Ryan, M.K. (1989). A GABA-immunoreactive synaptic plexus in the nerve fiber layer of primate retina. Visual Neuroscience 2, 19–25.CrossRefGoogle ScholarPubMed
Lipton, S. (1989). GABA-activated single-channel currents in outsideout membrane patches from rat retinal ganglion cells. Visual Neuroscience 3, 275–279.CrossRefGoogle ScholarPubMed
Maguire, G., Maple, B., Lukasiewicz, P. & Werblin, F. (1989). Gamma-aminobutyrate type B receptor modulation of L-type calcium channel current at bipolar cell terminals in the retina of the tiger salamander. Proceedings of the National Academy of Sciences of the U.S.A. 86, 10144–10147.CrossRefGoogle ScholarPubMed
Marc, R.E. (1986). Neurochemical stratification in the inner plexiform layer of the vertebrate retina. Vision Research 26, 223–238.CrossRefGoogle ScholarPubMed
Mariani, A.P. (1984). The neuronal organization of the outer plexiform layer of the primate retina. International Review of Cytology 86, 285–320.CrossRefGoogle ScholarPubMed
Mariani, A.P. & Caserta, M.T. (1986). Electron microscopy of glutamate decarboxylase (GAD) immunoreactivity in the inner plexiform layer of the rhesus monkey retina. Journal of Neurocytology 15, 645–655.CrossRefGoogle ScholarPubMed
Mariani, A.P. & Hersh, L.B. (1988). Synaptic organization of cholinergic amacrine cells in the rhesus monkey retina. Journal of Comparative Neurology 267, 269–280.CrossRefGoogle ScholarPubMed
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
Marshak, D. (1989). Peptidergic neurons of the macaque monkey retina. Neuroscience Research (Suppl.) 10, S117–S130.Google ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in cat retina. Journal of Neuroscience 4, 2920–2938.CrossRefGoogle ScholarPubMed
Morgan, W.W. (1985). GABA: a potential neurotransmitter in retina. In Retinal Transmitters and Modulators: Models for the Brain, Vol. 2, ed. Morgan, W.W., pp. 63–96. Boca Raton, FL: CRC Press.Google Scholar
Mosinger, J.L. & Altschuler, R.A. (1985). Aspartate aminotransferase-like immunoreactivity in the guinea pig and monkey retinas. Journal of Comparative Neurology 233, 255–268.CrossRefGoogle ScholarPubMed
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
Muller, J.F. & Marc, R.E. (1990). GABAergic and glycinergic pathways in the inner plexiform layer of the goldfish retina. Journal of Comparative Neurology 291, 281–304.CrossRefGoogle ScholarPubMed
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Nakamura, Y., McGuire, B.A. & Sterling, P. (1980). Interplexiform cell in cat retina: identification by uptake of gamma-[3H]aminobutyric acid. Proceedings of the National Academy of Sciences of the U.S.A. 77, 658–661.CrossRefGoogle Scholar
Nelson, R., Kolb, H., Chandler, N. & DeKorver, L. (1989). Neural circuitry of OFF-alpha and OFF-beta ganglion cells in cat retina. Investigative Ophthalmology and Visual Science (Suppl.) 30, 69.Google Scholar
Nishimura, Y., Schwartz, M.L. & Rakic, P. (1985). Localization of gamma-aminobutyric acid and glutamic acid decarboxylase in rhesus monkey retina. Brain Research 359, 351–355.CrossRefGoogle ScholarPubMed
Ottersen, O.P. (1989). Quantitative electron-microscopic immunocytochemistry of neuroactive amino acids. Anatomy and Embryology 180, 1–15.CrossRefGoogle ScholarPubMed
Owczarzak, M.T. & Pourcho, R.G. (1989). Glycine immunoreactivity in the cat retina: comparison and colocalization with GABA. Investigative Ophthalmology and Visual Science (Suppl.) 30, 121.Google Scholar
Owczarzak, M.T., Goebel, D.J. & Pourcho, R.G. (1988). Light- and electron-microscopic immunocytochemical localization of GABA in the cat retina. Investigative Opthalmology and Visual Science (Suppl.) 29, 197.Google Scholar
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.CrossRefGoogle Scholar
Polyak, S.L. (1941). The Retina. Chicago, Illinois: University of Chicago Press.Google Scholar
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, 25–35.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
Pritchett, D.B., Sontheimer, H., Shivers, B.D., Ymer, S., Kettenmann, H., Schofield, P.R. & Seeburg, P.H. (1989). Importance of a novel GABAA receptor subunit for benzodiazepine pharmacology. Nature 338, 582–585.CrossRefGoogle ScholarPubMed
Raviola, G. & Raviola, E. (1967). Light- and electron-microscopic observations on the inner plexiform layer of the rabbit retina. American Journal of Anatomy 120, 403–426.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1989). Starburst amacrines of the primate retina. Journal of Comparative Neurology 285, 18–37.CrossRefGoogle ScholarPubMed
Ryan, M.K. & Hendrickson, A.E. (1987). Interplexiform cells in macaque monkey retina. Experimental Eye Research 45, 57–66.CrossRefGoogle ScholarPubMed
Sakai, H.M., Naka, K.-I. & Dowling, J.E. (1986). Ganglion cell dendrites are presynaptic in catfish retina. Nature 319, 495–497.CrossRefGoogle ScholarPubMed
Sarthy, P.V. & Fu, M. (1989). 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
Sarthy, P.V., Hendrickson, A.E. & Wu, J.-W. (1986). L-glutamate: a neurotransmitter candidate for cone photoreceptors in the monkey retina. Journal of Neuroscience 6, 637–643.CrossRefGoogle ScholarPubMed
Tachibana, M. & Kaneko, A. (1988). Retinal bipolar cells receive negative feedback from GABAergic amacrine cells. Visual Neuroscience 1, 297–305.CrossRefGoogle ScholarPubMed
Tauck, D.L., Frosch, M.P. & Lipton, S.A. (1988). Characterization of GABA- and glycine-induced currents of solitary rodent retinal ganglion cells in culture. Neuroscience 27, 193–204.CrossRefGoogle ScholarPubMed
Vaney, D.I. & Young, H.M. (1988). GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Research 438, 369–373.CrossRefGoogle ScholarPubMed
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, 113–127.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
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434–454.CrossRefGoogle ScholarPubMed
Watanabe, M., Fukuda, Y., Hsiao, C.-F. & Ito, H. (1985). Electron-microscopic analysis of amacrine and bipolar inputs on Y, X, and W cells in the cat retina. Brain Research 358, 229–240.CrossRefGoogle Scholar
Weber, A.J., McCall, M.A. & Stanford, L.R. (1989). Synaptic input to a physiologically identified X cell in the cat retina. Society for Neuroscience Abstracts 15, 925.Google Scholar
Yazulla, S. (1981). GABAergic synapses in the goldfish retina: an auto-radiographic study of [3H]-muscimol and [3H]-GABA binding. Journal of Comparative Neurology 200, 83–93.CrossRefGoogle Scholar
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.CrossRefGoogle Scholar
Yazulla, S. & Yang, C.-Y. (1988). Colocalization of GABA and glycine immunoreactivities in a subset of retinal neurons in tiger salamander. Neuroscience Letters 95, 37–41.CrossRefGoogle Scholar
Yazulla, S., Studholme, K.M. & Wu, J.-Y. (1987). GABAergic input to the synaptic terminals of mbl bipolar cells in the goldfish retina. Brain Research 411, 400–405.CrossRefGoogle Scholar
Yu, B.C.-Y., Watt, C.B., Lam, D.M.K. & Fry, K.R. (1988). GABAergic ganglion cells in the rabbit retina. Brain Research 439, 376–382.CrossRefGoogle ScholarPubMed