Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-24T12:33:47.835Z Has data issue: false hasContentIssue false
  • English
  • Français

Glutamate-, GABA-, and GAD-immunoreactivities co-localize in bipolar cells of tiger salamander retina

Published online by Cambridge University Press:  02 June 2009

Chen-Yu Yang  and
Stephen Yazulla
Chen-Yu Yang
Affiliation:
Department of Neurobiology and Behavior, University at Stony Brook, Stony Brook
Stephen Yazulla
Affiliation:
Department of Neurobiology and Behavior, University at Stony Brook, Stony Brook
Get access Rights & Permissions [Opens in a new window]

Abstract

The presence of inhibitory bipolar cells in salamander retina was investigated by a comparative analysis of the distribution of glutamate- and GABA-immunoreactivities (GLU-IR; GABA-IR) using a postembedding immunocytochemical method. GLU-IR was found in virtually all photoreceptors, bipolar cells and ganglion cells, neuronal elements that transfer information vertically through the retina. GLU-IR also was found in numerous amacrine cells in the mid and proximal inner nuclear layer as well as in the cytoplasm of horizontal cells, while the nucleus of horizontal cells was either lightly labeled or not labeled at all. GLU-IR was found in the outer plexiform layer and intensely in the inner plexiform layer, in which there was no apparent sublamination. Forty-seven percent of Type IB bipolar cells in the distal inner nuclear layer and 13% of the displaced bipolar cells were GABA-IR. All bipolar cells were also GLU-IR, indicating that GABA-IR bipolar cells were a subset of GLU-IR bipolar cells rather than a separate population. About 12% of the Type IB bipolar cells were moderately GABA-IR and likely comprised a GABAergic subtype. GLU-IR levels in the presumed GABAergic bipolar cells were higher than in other purely GLU-IR bipolar cells suggesting that these GABA-IR bipolar cells are glutamatergic as well. All of the displaced bipolar cells were only lightly GABA-IR, indicating that displaced bipolar cells comprise a more homogeneous class of glutamatergic cell than orthotopic bipolar cells. GAD-IR co-localized with GABA-IR in orthotopic but not displaced bipolar cells, further supporting the idea that some orthotopic bipolar cells are GABAergic. A small proportion of bipolar cells in salamander retina contain relatively high levels of both GABA and glutamate. Co-release of these substances by bipolar cells could contribute to the “push-pull” modulation of ganglion cell responses.

Keywords

RetinaSalamanderBipolar cellsGlutamateGABAGAD
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 6 , November 1994 , pp. 1193 - 1203
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., Ekstroem, P., Van Veen, T. & Wu, J. (1987 a). 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. & Wu, J.-Y. (1987 b). GABA and GAD-like immunoreactivity in the primate retina. Histochemistry 86, 485–490.CrossRefGoogle ScholarPubMed
Arkin, M.S. & Miller, R.F. (1988 a). Synaptic inputs and morphology of sustained ON-ganglion cells in the mudpuppy retina. Journal of Neurophysiology 60, 1143–1159.CrossRefGoogle ScholarPubMed
Arkin, M.S. & Miller, R.F. (1988 b). Bipolar origin of synaptic inputs to sustained OFF-ganglion cells in the mudpuppy retina. Journal of Neurophysiology 60, 1122–1142.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1982). Sustained synaptic input to ganglion cells of mudpuppy retina. Journal of Physiology (London) 326, 91–108.CrossRefGoogle ScholarPubMed
Belgum, J.H., Dvorak, D.R. & McReynolds, J.S. (1984). Strychnine blocks transient but not sustained inhibition in mudpuppy retinal ganglion cells. Journal of Physiology (London) 354, 273–286.CrossRefGoogle Scholar
Bradford, H.F., Docherty, M., Wu, J.Y., Cash, C.D., Ehret, M., Maitre, M. & Joh, T.H. (1989). The immunolysis, isolation and properties of subpopulations of mammalian brain synaptosomes. Neurochemical Research 14, 301–310.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
Cohen, E. & Sterling, P. (1986). Accumulation of 3H-glycine by cone bipolar neurons in the cat retina. Journal of Comparative Neurology 250, 1–7.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 immunocyto-chemical investigation. Journal of Comparative Neurology 311, 483–494.CrossRefGoogle Scholar
Dixon, D.B. & Copenhagen, D.R. (1992). Two types of glutamate receptors differentially excite amacrine cells in the tiger salamander retina. Journal of Physiology (London) 449, 589–606.CrossRefGoogle ScholarPubMed
Dowling, J.E. (1987). The Retina: An Approachable Part of the Brain. Cambridge, Massachusetts: Harvard University Press.Google Scholar
Ehinger, B., Ottersen, O.P., Storm-Mathisen, J. & Dowling, J.E. (1988). Bipolar cells in the turtle retina are strongly immunoreactive for glutamate. Proceedings of the National Academy of Sciences of the U.S.A. 85, 8321–8325.CrossRefGoogle ScholarPubMed
Gábriel, R., Straznicky, C. & Wye-Dvorak, J. (1992). GABA-like immunoreactive neurons in the retina of Bufo marinus: Evidence for the presence of GABA-containing ganglion cells. Brain Research 571, 175–179.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
Hare, W.A., Lowe, J.S. & Owen, G. (1986). Morphology of physiologically identified bipolar cells in the retina of the tiger salamander, Ambystoma tigrinum. Journal of Comparative Neurology 252, 130–138.CrossRefGoogle ScholarPubMed
Hensley, S.H., Yang, X.-L. & Wu, S.M. (1993). Identification of glutamate receptor subtypes mediating inputs to bipolar cells and ganglion cells in the tiger salamander retina. Journal of Neurophysiology 69, 2099–2107.CrossRefGoogle ScholarPubMed
Hickmott, P.W. & Constanttne-Paton, M. (1993). The contributions of NMDA, non-NMDA, and GABA receptors to postsynaptic responses in neurons of the optictectum. Journal of Neuroscience 13, 4339–4353.CrossRefGoogle Scholar
Hurd, L.B. II. & Eldred, W.D. (1989). Localization of GABA- and GAD-like immunoreactivity in the turtle retina. Visual Neuroscience 3, 9–20.CrossRefGoogle ScholarPubMed
Kageyama, G.H. & Meyer, R.L. (1989). Glutamate-immunoreactivity in the retina and optic tectum of goldfish. Brain Research 503, 118–127.CrossRefGoogle ScholarPubMed
Kalloniatis, M. & Fletcher, E.L. (1993). Immunocytochemical localization of the amino acid neurotransmitters in the chicken retina. Journal of Comparative Neurology 336, 174–193.CrossRefGoogle ScholarPubMed
Kim, H.G. & Miller, R.F. (1991). Rods and cones activate different excitatory amino acid receptors on the mudpuppy retinal horizontal cell. Brain Research 538, 141–146.CrossRefGoogle ScholarPubMed
Kim, H.G. & Miller, R.F. (1993). Properties of synaptic transmission from photoreceptors to bipolar cells in the mudpuppy retina. Journal of Neurophysiology 69, 352–360.CrossRefGoogle ScholarPubMed
Levine, M.W. & Shefner, J.M. (1977). Variability in ganglion cell firing patterns: Implications for separate ON and OFF processes. Vision Research 17, 765–776.CrossRefGoogle ScholarPubMed
Li, T., Wu, S.M., Lam, D.M.K. & Watt, C.B. (1990). Localization of classical neurotransmitters in interneurons of the larval tiger salamander retina. Investigative Ophthalmology and Visual Science 31, 262–271.Google ScholarPubMed
Lugo-Garcia, N. & Blanco, R.E. (1991). Localization of GAD- and GABA-like immunoreactivity in ground squirrel retina: Retrograde labeling demonstrates GAD-positive ganglion cells. Brain Research 564, 19–26.CrossRefGoogle ScholarPubMed
Lukasiewicz, P.D. & McReynolds, J.S. (1985). Synaptic transmission at the N-methyl-D-aspartate receptors in the proximal retina of the mudpuppy. Journal of Physiology (London) 367, 99–115.CrossRefGoogle ScholarPubMed
Marc, R.E., Liu, W.L.S., Kalloniatis, M., Raiguel, S.F. & Van Haesendonck, E. (1990). Patterns of glutamate immunoreactivity in the goldfish retina. Journal of Neuroscience 10, 4006–4034.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 Neurocylology 15, 645–655.Google ScholarPubMed
Martin, P.R. & Grünert, U. (1992). Spatial density and immunoreactivity of bipolar cells in the macaque monkey retina. Journal of Comparative Neurology 323, 269–287.CrossRefGoogle ScholarPubMed
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. Progress in Retinal Research 9, 399–425.CrossRefGoogle Scholar
McGuire, B.A., Stevens, J.K. & Sterling, P. (1984). Microcircuitry of bipolar cells in cat retina. Journal of Neuroscience 4, 2920–2938.CrossRefGoogle ScholarPubMed
McGuire, B.A., Stevens, J.K. & Sterling, P. (1986). Microcircuitry of beta ganglion cells in cat retina. Journal of Neuroscience 6, 907–918.CrossRefGoogle ScholarPubMed
McReynolds, J.S. & Lukasiewicz, P.D. (1989). Integration of synaptic input from ON and OFF pathways in the mudpuppy retinal ganglion cells. In Neurobiology of the Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 209–220. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Mittman, S., Taylor, W.R. & Copenhagen, D.R. (1990). Concomitant activation of two types of glutamate receptor mediates excitation of salamander retinal ganglion cells. Journal of Physiology (London) 428, 175–197.CrossRefGoogle ScholarPubMed
Mosinger, J.L., Studholme, K.M. & Yazulla, S. (1986). Immunocytochemical localization of GABA in the retina: A species comparison. Experimental Eye Research 42, 631–644.CrossRefGoogle Scholar
Müller, F., Wässle, H. & Voigt, T. (1988). Pharmacological modulation of rod pathway in the cat retina. Journal of Neurophysiology 59, 1657–1672.CrossRefGoogle ScholarPubMed
Neal, M.J., Cunningham, J.R. & Shah, M.A. (1989). Excitatory amino acid receptors and transmitter release in the retina. Neurochemistry International 4, 407–412.CrossRefGoogle Scholar
Neal, M.J. & Cunningham, J.R. (1989). L-Homocysteic acid–a possible bipolar cell transmitter in the rabbit retina. Neuroscience Letters 102, 114–119.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 1183–1195.CrossRefGoogle ScholarPubMed
Oertel, W.H., Schmechel, D.E., Tappaz, M.A. & Kopin, I.J. (1981). Production of a specific antiserum to rat brains glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6, 2689–2700.CrossRefGoogle ScholarPubMed
Osborne, N.N., Patel, S., Beaton, D.W. & Neuhoff, V. (1986). GABA neurones in retinas of different species and their postnatal development in situ and in culture in the rabbit retina. Cell and Tissue Research 243, 117–123.CrossRefGoogle ScholarPubMed
Pourcho, R.G., Goebel, D.J. & McReynolds, J.S. (1984). Autoradiographic studies of [3H]-glycine, [3H]-GABA, and [3H]-muscimol uptake in the mudpuppy retina. Experimental Eye Research 39, 69–81.CrossRefGoogle Scholar
Pourcho, R.G. & Goebel, D.J. (1987 a). A combined Golgi and auto-radiographic study of 3H-glycine-accumulating cone bipolar cells in the cat retina. Journal of Neuroscience 7, 1178–1188.CrossRefGoogle Scholar
Pourcho, R.G. & Goebel, D.J. (1987 b). Visualization of endogenous glycine in cat retina: An immunocytochemical study with Fab fragments. Journal of Neuroscience 7, 1189–1197.CrossRefGoogle ScholarPubMed
Pourcho, R.G. & Owczarzak, M.T. (1991). Glycine receptor immunoreactivity is localized at amacrine synapses in cat retina. Visual Neuroscience 7, 611–618.CrossRefGoogle ScholarPubMed
Sherry, D.M. & Ulshafer, R.J. (1992). Neurotransmitter-specific identification and characterization of neurons in the all-cone retina of Anolis carolinensis. II. Glutamate and aspartate. Visual Neuroscience 9, 313–323.CrossRefGoogle ScholarPubMed
Slaughter, M.M., Bai, S.H. & Pan, Z.H. (1989). Desegregation: Bussing of signals through the retinal network. In Neurobiology of Inner Retina, ed. Weiler, R. & Osborne, N.N., pp. 335–347. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid: A new pharmacological tool for retina research. Science 211, 182–185.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1983). Bipolar cells in the mud-puppy retina use an excitatory amino acid neurotransmitter. Nature 303, 537–539.CrossRefGoogle Scholar
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.CrossRefGoogle ScholarPubMed
Su, Y.Y. T., Wu, J.-Y. & Lam, D.M.K. (1979). Purification of L-glutamic acid decarboxylase from catfish brain. Journal of Neurochemistry 33, 169–179.Google ScholarPubMed
Toyoda, J., Shimbo, K., Kondo, H. & Kujiraoka, T. (1992). Push-pull modulation of ganglion cell responses of carp retina by amacrine cells. Neuroscience Letters 142, 41–44.CrossRefGoogle ScholarPubMed
Van Haesendonck, E. & Missotten, L. (1990). Glutamate-like immunoreactivity in the retina of a marine teleost, the dragonet. Neuroscience Letters 111, 281–286.CrossRefGoogle ScholarPubMed
Van Haesendonck, E. & Missotten, L. (1993). A subgroup of bipolar cells in human retina is GABA-immunoreactive. Neuroscience Letters 161, 187–190.CrossRefGoogle ScholarPubMed
Voaden, M.J., Marshall, J. & Murani, N. (1974). The uptake of 3H-GABA and 3H-glycine by the isolated retina of the frog. Brain Research 67, 115–132.CrossRefGoogle Scholar
Wässle, H., Schäfer-Trenkler, I. & Voigt, T. (1986). Analysis of a glycinergic inhibitory pathway in the cat retina. Journal of Neuroscience 6, 594–604.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
Wenthold, R., Zemple, J., Parakkal, M.A., Reeks, K.A. & Alt-Schuler, R.A. (1986). Immunocytochemical localization of GABA in the cochlear nucleus of the guinea pig. Brain Research 380, 7–18.CrossRefGoogle ScholarPubMed
Werblin, F.S., Maguire, G.W., Lukasiewicz, P.O., Eliasof, S.R. & Wu, S. (1988). Neural interations mediating the detection of motion in the retina of the tiger salamander. Visual Neuroscience I, 317–329.CrossRefGoogle Scholar
Werblin, F.S. & Dowling, J.E. (1969). Organization of the retina of the mudpuppy, II. Intracellular recording. Journal of Neurophysiology 32, 355.CrossRefGoogle ScholarPubMed
White, L.E., Hodges, H.D., Carnes, K.M., Price, J.L. & Dubinsky, J.M. (1994). Co-localization of excitatory and inhibitory neurotransmitter markers in striatal projection neurons in the rat. Journal of Comparative Neurology 339, 328–340.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Yang, C.Y. & Yazulla, S. (1988 a). Localization of putative GABAergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographic methods. Journal of Comparative Neurology 277, 96–108.CrossRefGoogle ScholarPubMed
Yang, C.Y. & Yazulla, S. (1988 b). Light microscopic localization of putative glycinergic neurons in the larval tiger salamander retina by immunocytochemical and autoradiographical methods. Journal of Comparative Neurology 272, 343–357.CrossRefGoogle ScholarPubMed
Yang, C.Y. & Yazulla, S. (1993). Glutamate- and GABA-immuno-reactivities in retinal bipolar cells of tiger salamander. Society for Neuroscience Abstracts 19, 115.Google Scholar
Yang, X.L. & Wu, S.M. (1989). Effects of CNQX, APB, PDA, and kynurenate on horizontal cells of the tiger salamander retina. Visual Neuroscience 3, 207–212.CrossRefGoogle ScholarPubMed
Yazulla, S. (1986). GABAergic mechanisms in the retina. Progress in Retinal Research 5, 1–52.CrossRefGoogle Scholar
Zhu, B.-S. & Straznicky, C. (1993). Co-localization of serotonin and GABA in neurons of the Xenopus laevis retina. Anatomical Embryology 187, 549–555.CrossRefGoogle ScholarPubMed