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Localization of AMPA-selective glutamate receptor subunits in the adult cat visual cortex

Published online by Cambridge University Press:  02 June 2009

K. Gutiérrez-Igarza ,
D. J. Fogarty ,
F. Pérez-Cerdá ,
F. Doñate-Oliver ,
K. Albus  and
C. Matute
K. Gutiérrez-Igarza
Affiliation:
Departamento de Neurociencias, Universidad del Pais Vasco, 48940 Leioa, Spain
D. J. Fogarty
Affiliation:
Departamento de Neurociencias, Universidad del Pais Vasco, 48940 Leioa, Spain
F. Pérez-Cerdá
Affiliation:
Departamento de Neurociencias, Universidad del Pais Vasco, 48940 Leioa, Spain
F. Doñate-Oliver
Affiliation:
Departamento de Neurociencias, Universidad del Pais Vasco, 48940 Leioa, Spain
K. Albus
Affiliation:
Abteilung Neurobiologie, Max Planck Institut für Biophysikalische Chemie, Am Faßberg, 37018 Göttingen, Germany
C. Matute
Affiliation:
Departamento de Neurociencias, Universidad del Pais Vasco, 48940 Leioa, Spain
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Abstract

We have studied the presence and distribution of α-amino-3–hydroxy-5–methyl-4–isoxazolepropionate (AMPA)-selective glutamate receptor subunits (GluR 1, 2, 3, and 4) in the adult cat visual cortical areas 17, 18, 19, and the lateral suprasylvian areas (LSA). Reverse transcription-polymerase chain reaction (RT-PCR) amplification indicated that the genes encoding GluR 1, 2, 3, and 4 are expressed in these areas and Western blot analysis revealed that the size of the corresponding peptides is similar to those described in the rat brain. In situ hybridization (ISH) using digoxigenin-labeled riboprobes showed that mRNAs coding for GluR1 and GluR3 were located in cells in all layers of the areas examined and also in the underlying white matter. GluR1 mRNA was relatively abundant throughout layers II–VI while GluR3 mRNA revealed a more laminated pattern of expression, preferentially labeling cells in layers II, III, V, and VI. The distribution of AMPA-selective receptor subunit peptides was studied by immunohistochemistry using subunit specific antibodies and found to be consistent with ISH results. In addition, we observed that most of the cells strongly labeled by the anti-GluR1 antibody were non-pyramidal neurons and that intense GluR2/3 immunoreactivity was seen preferentially in pyramidal neurons. Interestingly, double-labeling experiments indicated that neurons expressing γ-aminobutyric acid (GABA) as well as the GluR1 subunit were particularly abundant in deeper layers. The GluR4 peptide was predominantly found in a relatively low number of layer III and layer V neurons with either pyramidal or non-pyramidal morphology. Finally, the distribution of neurons expressing the various receptor subunits was similar in all the visual cortical areas studied. These findings indicate a high expression of GluR1–3 subunits in the cat visual cortex and that GluR1 and GluR2/3 subunits are particularly abundant in non-pyramidal and pyramidal neurons, respectively. In addition, the results described here provide a reference for future studies dealing with the effect of visual deprivation on the expression of this receptor type.

Keywords

RT-PCRIn situ hybridizationImmunohistochemistryOccipital cortexExcitatory amino acid receptors

Information

Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 1 , January 1996 , pp. 61 - 72
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Bliss, T.V.P. & Collingridge, G.L. (1993). A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361, 31–39.CrossRefGoogle ScholarPubMed
Bochet, P., Audinat, E., Lambolez, B., Crepel, F., Rossier, J., Ilno, M., Tsuzuki, K. & Ozawa, S. (1994). Subunit composition at the single-cell level explains functional properties of a glutamate-gated channel. Neuron 12, 383–388.Google Scholar
Briarty, L.G. (1975). Stereology: Methods for quantitative light and electron microscopy. Science Progress (Oxford) 62, 1–32.Google ScholarPubMed
Cajaraville, M.P., Marigomez, J.A. & Angulo, E. (1991). Automated measurement of lysosomal structure alterations in oocytes of mussels exposed to petroleum hydrocarbons. Archives of Environmental Contamination and Toxicology 21, 395–400.CrossRefGoogle ScholarPubMed
Choi, D.W. (1988). Glutamate neurotoxicity and diseases of the nervous system. Neuron 1, 623–634.CrossRefGoogle ScholarPubMed
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156–159.CrossRefGoogle ScholarPubMed
Cotman, C.W., Monaghan, D.T., Ottersen, O.P. & Storm-Mathisen, J. (1987). Anatomical organization of excitatory amino acid receptors and their pathways. Trends in Neurosciences 10, 273–279.CrossRefGoogle Scholar
Demeulemeester, H., Vandensande, F., Orban, G.A. & Van-derhaughen, J.J. (1988). Heterogeneity of GABAergic cells in cat visual cortex. Journal of Neuroscience 8, 988–1000.CrossRefGoogle ScholarPubMed
Dori, I., Dinopoulos, A., Cavanagh, M.E. & Parnavelas, J.G. (1992). Proportion of glutamate- and aspartate-immunoreactive neurons in the efferent pathways of the rat visual cortex varies according to the target. Journal of Comparative Neurology 319, 191–204.CrossRefGoogle ScholarPubMed
Fogarty, D.J., Gutierrez-Igarza, K., Doñate, F., Albus, K. & Matute, C. (1993). Distribution of AMPA/kainate receptor mRNAs in the adult cat visual system. European Journal of Neuroscience (Suppl.) 7, 133 (Abstract).Google Scholar
Gallo, V., Upson, L.M., Hayes, W.P., Vyklicky, L. Jr, Winters, C.A. & Buonanno, A. (1992). Molecular cloning and developmental analysis of a new glutamate receptor subunit isoform in cerebellum. Journal of Neuroscience 12, 1010–1023.CrossRefGoogle Scholar
Hollmann, M. & Heinemann, S. (1994). Cloned glutamate receptors. Annual Reviews of Neuroscience 17, 31–108.Google Scholar
Hollmann, M., O'Shea-Greenfield, A., Rogers, S.W. & Heinemann, S. (1989). Cloning by functional expression of a member of the glutamate receptor family. Nature 342, 643–648.CrossRefGoogle ScholarPubMed
Huntley, G.W., Rogers, S.W., Moran, T., Jansen, W., Archin, N., Vickers, J.C., Cauley, K., Heinemann, S.R & Morrison, J.H. (1993). Selective distribution of kainate receptor subunit immuno-reactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. Journal of Neuroscience 13, 2965–2981.CrossRefGoogle Scholar
Innocenti, G.M. (1986). General organization of callosal connections in the cerebral cortex. In The Cerebral Cortex, Vol. 5, ed. Jones, E.G. & Peters, A., pp. 291–354. New York: Plenum.Google Scholar
Insel, T.R., Miller, L.P. & Gelhard, R.E. (1990). The ontogeny of excitatory amino acid receptors in rat forebrain –I. N-methyl-D-aspartate and quisqualate receptors. Neuroscience 35, 31–43.Google Scholar
Jensen, A.M. & Cmu, S.Y. (1993). Expression of glutamate receptor genes in white matter: Developing and adult rat optic nerve. Journal of Neuroscience 13, 1664–1675.CrossRefGoogle ScholarPubMed
Johnson, R.R. & Burkhalter, A. (1994). Evidence for excitatory amino acid neurotransmitters in forward and feedback cortico-cortical pathways within rat visual cortex. European Journal of Neuroscience 6, 272–286.CrossRefGoogle Scholar
Jonas, P., Racca, C., Sakmann, B., Seeburg, P.H. & Monyer, H. (1994). Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12, 1281–1289.CrossRefGoogle ScholarPubMed
Jones, K.A. & Baughman, R.W. (1988). NMDA- and non-NMDA-receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex. Journal of Neuroscience 8, 3522–3534.CrossRefGoogle Scholar
Kaufman, E.S. & Rosenquist, A.C. (1985). Efferent projections of the thalamic intralaminar nuclei in the cat. Brain Research 335, 252–279.Google ScholarPubMed
Kawaguchi, Y. (1992). Receptor subtypes involved in callosally-induced postsynaptic potentials in rat frontal agranular cortex in vitro. Experimental Brain Research 88, 33–40.CrossRefGoogle ScholarPubMed
Keinanen, K., Wisen, W., Sommer, B., Werner, P., Herb, A., Verdoorn, T.A., Sakmann, B. & Seeburg, P.H. (1990). A family of AMPA-selective glutamate receptors. Science 249, 556–560.CrossRefGoogle ScholarPubMed
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
Larson-Prior, L.J., Ulinski, P.S. & Slater, N.T. (1991). Excitatory amino acid receptor-mediated transmission in geniculocortical and intracortical pathways within visual cortex. Journal of Neurophysiology 66, 293–306.Google Scholar
Levay, S. (1986). Synaptic organization of claustral and geniculate afferents to the visual cortex of the cat. Journal of Neuroscience 6, 3564–3575.Google Scholar
Martin, L.J., Blackstone, C.D., Levey, A.I., Huganir, R.L. & Price, D.L. (1993). AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53, 327–358.CrossRefGoogle ScholarPubMed
Matute, C. & Streit, P. (1985). Selective retrograde labeling with D-3H aspartate in afferents to mammalian superior colliculus. Journal of Comparative Neurology 241, 34–49.Google Scholar
Matute, C. & Streit, P. (1986). Monoclonal antibodies demonstrating GABA-like immunoreactivity. Histochemistry 86, 147–157.CrossRefGoogle ScholarPubMed
Matute, C. & Miledi, R. (1993). Neurotransmitter receptors and voltage-dependent Ca2+ channels encoded by mRNA from the adult corpus callosum. Proceedings of the National Academy of Sciences of the U.S.A. 90, 3270–3274.CrossRefGoogle ScholarPubMed
Matute, C., Nguyen, Q.T. & Miledi, R. (1993 a). mRNAs coding for neurotransmitter receptors in rabbit and rat visual areas. Journal of Neuroscience Research 35, 652–663.CrossRefGoogle ScholarPubMed
Matute, C., Wahle, P., Gutierrez-Igarza, K. & Albus, K. (1993 b). Distribution of neurons expressing substance P receptor messenger RNA in immature and adult cat visual cortex. Experimental Brain Research 97, 295–300.CrossRefGoogle ScholarPubMed
McGlade-McCulloh, E., Yamamoto, H., Tan, S.-E., Brickey, D.A. & Soderling, T.R. (1993). Phosphorylation and regulation of glutamate receptors by calcium/calmodulin-dependent protein kinase II. Nature 362, 640–642.Google Scholar
Otsuka, R. & Hassler, R. (1962). Über Aufbau und Gliederung der Corticalen Sehsphäre bei der Katze. Archiv für Psychiatrie und Zeit-schrift für des Gesseischaft Neurologic 203, 212–234.CrossRefGoogle Scholar
Pellegrini-Giampietro, D.E., Bennett, M.V.L. & Zukin, R.S. (1991). Differential expression of three glutamate receptor genes in developing rat brain: An in situ hybridization study. Proceedings of the National Academy of Sciences of the U.S.A. 88, 4157–4161.CrossRefGoogle Scholar
Pérez-Cerdá, R, Martinez-Millan, L. & Matute, C. (1989). Transporte de D-(3H)-aspartato (D-3H-AA) en las conexiones visuales del gato adulto. Resúmenes de publicaciones del III Congreso Nacional de la Sociedad de Neurociencias, Spain p. 223.Google Scholar
Petralia, R.S. & Wenthold, R.J. (1992). Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. Journal of Comparative Neurology 318, 329–354.CrossRefGoogle ScholarPubMed
Petralia, R.S., Yokotani, N. & Wenthold, R.J. (1994). Light and electron microscope distribution of the NMDA receptor subunit NMDARI in the rat nervous system using a selective anti-peptide antibody. Journal of Neuroscience 14, 667–696.Google Scholar
Puchalski, R.B., Louis, J.C., Brose, N., Traynelis, S.F., Egebjerg, J., Kukekov, V., Wenthold, R.J., Rogers, S.W., Lin, F., Moran, T., Morrison, J.H. & Heinemann, S.F. (1994). Selective RNA editing and subunit assembly of native glutamate receptors. Neuron 13, 131–147.Google Scholar
Rauschecker, J.P. (1991). Mechanisms of visual plasticity: Hebb synapses, NMDA receptors, and beyond. Physiological Reviews 71, 587–615.CrossRefGoogle ScholarPubMed
Roßner, S., Kumar, A., Kues, W., Witzemann, V. & Schliebs, R. (1993). Differential laminar expression of AMPA receptor genes in the developing rat visual cortex using hybridization histochemistry. Effect of visual deprivation. International Journal of Developmental Neuroscience 11, 411–424.Google ScholarPubMed
Rosenquist, A.C. (1985). Connections of visual cortical areas in the cat. In The Cerebral Cortex, Vol. 5, ed. Jones, E.G. & Peters, A. pp. 81–118. New York: Plenum.Google Scholar
Rusin, K.I., Jiang, M.C., Cerne, R. & Randic, M. (1993). Interactions between excitatory amino acids and tachykinins in the rat spinal dorsal hòrn. Brain Research Bulletin 30, 329–338.Google Scholar
Sato, K., Kiyama, H. & Tohyama, M. (1993). The differential expression patterns of messenger RNAs encoding non-N-methyl-D-aspartate glutamate receptor subunits (GluR1–4) in the rat brain. Neuroscience 52, 515–539.CrossRefGoogle ScholarPubMed
Shaw, C., Wilkinson, M., Cynader, M., Needler, M.C., Aoki, C. & Hall, S.E. (1986). The laminar distributions and postnatal development of neurotransmitter and neuromodulator receptors in cat visual cortex. Brain Research Bulletin 16, 661–671.CrossRefGoogle ScholarPubMed
Symonds, L.L., Rosenquist, A.C., Edwards, S.B. & Palmer, L.A. (1981). Projections of the pulvinar-lateral posterior complex to visual cortical areas in the cat. Neuroscience 6, 1995–2020.CrossRefGoogle ScholarPubMed
Thompson, A.M. & Deuchars, J. (1994). Temporal and spatial properties of local circuits in neocortex. Trends in Neurosciences 17, 119–130.CrossRefGoogle Scholar
Tsumoto, T. (1990). Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral cortex. Neuroscience Research 9, 79–102.CrossRefGoogle Scholar
Vickers, J.C., Huntley, G.W., Edwards, A.M., Moran, T., Rogers, S.W., Heinemann, S.F. & Morrison, J.H. (1993). Quantitative localization of AMPA/kainate and kainate glutamate receptor subunit immunoreactivity in neurochemically identified subpopulations of neurons in the prefrontal cortex of the macaque monkey. Journal of Neuroscience 13, 2982–2992.CrossRefGoogle ScholarPubMed
Weber, W., Bertics, P.J. & Gill, G.N. (1984). Immunoaffinity purification of the epidermal growth factor receptor. Stoichiometry of binding and kinetics of self-phosphorylation. Journal of Biological Chemistry 259, 14631–14636.Google Scholar
Wenthold, R.J., Yokotani, N., Doi, K. & Wada, K. (1992). Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. Journal of Biological Chemistry 267, 501–507.Google Scholar
White, E.L. (1986). Termination of thalamic afferents in the cerebral cortex. In The Cerebral Cortex, Vol. 5, ed. Jones, E.G. & Peters, A., pp. 271–290. New York: Plenum.Google Scholar