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Neuronal and glial localization of NMDA receptors in the cerebral cortex

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Abstract

The crucial role of glutamate receptors of theN-methyl-d-aspartate (NMDA) type in many fundamental cortical functions has been firmly established, as has its involvement in several neuropsychiatric diseases, but until recently, very little was known of the anatomical localization of NMDA receptors in the cerebral cortex of mammals. The recent application of molecular biological techniques to the study of NMDA receptors has allowed the production of specific tools, the use of which has much increased our understanding of the localization of NMDA receptors in the cerebral cortex. In particular, immunocytochemical studies on the distribution of cortical NMDA receptors have:

  1. 1.

    Demonstrated the preferential localization of NMDA receptors in dendritic spines, in line with previous work;

  2. 2.

    Disclosed a thus far unknown fraction of presynaptic NMDA receptors on both excitatory and inhibitory axon terminals; and

  3. 3.

    Shown that cortical astrocytes express NMDA receptors.

These studies indicate that the effects of cortical NMDA receptor activation are not caused exclusively by the opening of NMDA channels on neuronal postsynaptic membranes, as previously assumed, and that the activation of presynaptic and glial NMDA receptors can contribute significantly to these effects.

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References

  • Akbarian S., Sucher N. J., Bradley D., Tafazzoli A., Trinh D., Hetrick W. P., Potkin S. G., Sandman C. A., Bunney W. E. Jr., and Mones E. G. (1996) Selective alterations in gene expression for NMDA receptor subunits in prefrontal cortex of schizophrenics.J. Neurosci. 16, 19–30.

    PubMed  CAS  Google Scholar 

  • Aoki C., Venkatesan C., Go C.-G., Mong J. A., and Dawson T. M. (1994) Cellular and subcellular localization of NMDA-R1 subunit immunoreactivity in the visual cortex of adult and neonatal rats.J. Neurosci. 14, 5202–5222.

    PubMed  CAS  Google Scholar 

  • Aoki C., Fenstemaker S., Rhee J., Song X.-Z., Go C.-G., and Dawson T. M. (1996) Nitric oxide-synthesizing neurons in the cerebral cortex: anatomy and functional implications, inExcitatory Amino Acids and the Cerebral Cortex (Conti F. and Hicks T. P., eds.), MIT Press, Cambridge, MA, pp. 175–187.

    Google Scholar 

  • Armstrong-James M., Welker E., and Callahan C. A. (1993) The contribution of NMDA and non-NMDA receptors to fast and slow transmission of sensory information in the rat SI barrel cortex.J. Neurosci. 13, 2149–2160.

    PubMed  CAS  Google Scholar 

  • Benson D. L., Isackson P. J., Hendry S. H. C., and Jones E. G. (1989) Expression of glutamic acid decarboxylase mRNA in normal and monocularly deprived cat visual cortex.Mol. Brain Res. 5, 279–287.

    Article  PubMed  CAS  Google Scholar 

  • Benson D. L., Isackson P. J., Gall C. M., and Jones E. G. (1991) Differential effects of monocular deprivation on glutamic acid decarboxylase and type II calcium-calmodulin-dependent kinase gene expression in the adult monkey visual cortex.J. Neurosci. 11, 31–47.

    PubMed  CAS  Google Scholar 

  • Blankenfeld V. G., Enkuist K., and Kettenmann H. (1995) Gamma-aminobutyric acid and glutamate receptors, inNeuroglia. (Kettenmann H. and Ransom B., eds.), Oxford University Press, New York, pp. 335–345.

    Google Scholar 

  • Bliss T. V. P. and Collingridge G. L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus.Nature 361, 31–39.

    Article  PubMed  CAS  Google Scholar 

  • Bustos G., Abarca J., Forray M. I., Gysling K., Bradberry C. W., and Roth R. H. (1992) Regulation of excitatory amino acid release byN-methyl-d-aspartate receptors in rat striatum: in vivo microdialysis studies.Brain Res. 585, 105–115.

    Article  PubMed  CAS  Google Scholar 

  • Cajal, S. Ramon, Y. (1911)Histologie du Système Nerveux de l'Homme et des Vertébrés. Maloine, Paris.

    Google Scholar 

  • Chernevskaya N. I., Obokhov A. G., and Kristhal O. A. (1991) NMDA receptor agonists selectively block N-type calcium channels in hippocampal neurons.Nature 349, 418–420.

    Article  PubMed  CAS  Google Scholar 

  • Ciabarra A. M., Sullivan J. M., Gahn L. G., Pecht G., Heinemann S., and Sevarino K. A. (1995) Cloning and characterization of X-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family.J. Neurosci. 15, 6498–6508.

    PubMed  CAS  Google Scholar 

  • Cik M., Chazot P. L., and Stephenson F. A. (1993) Optimal expression of cloned NMDAR1/NMDAR2 heteromeric glutamate receptors: a biochemical characterization.Biochem. J. 296, 877–883.

    PubMed  CAS  Google Scholar 

  • Collingridge G. L. and Watkins J. C. (1994)The NMDA Receptor. Oxford University Press, Oxford.

    Google Scholar 

  • Conti F. and Hicks T. P. (1996)Excitatory Amino Acids and the Cerebral Cortex. MIT Press, Cambridge, MA.

    Google Scholar 

  • Conti F. and Minelli A. (1996) The anatomy of glutamatergic transmission, inExcitatory Amino Acids and the Cerebral Cortex. (Conti F. and Hicks T. P., eds.), MIT Press, Cambridge, MA, pp. 81–98.

    Google Scholar 

  • Conti F., Rustioni A., Petrusz P., and Towle A. C. (1987) Glutamate-positive neurons in the somatic sensory cortex of rats and monkeys.J. Neurosci. 7, 1887–1901.

    PubMed  CAS  Google Scholar 

  • Conti F., Fabri M., and Manzoni T. (1988) Glutamate-positive cortico-cortical neurons in the somatic sensory areas I and II of cats.J. Neurosci. 8, 2948–2960.

    PubMed  CAS  Google Scholar 

  • Conti F., DeFelipe J., Farinas I., and Manzoni T. (1989) Glutamate-positive neurons and axon terminals in cat sensory cortex: a correlative light and electron microscopic study.J. Comp. Neurol. 290, 141–153.

    Article  PubMed  CAS  Google Scholar 

  • Conti F., DeBiasi S., Fabri M., and Manzoni T. (1992) Substance P-containing pyramidal neurons in the cat somatic sensory cortex.J. Comp. Neurol. 322, 136–148.

    Article  PubMed  CAS  Google Scholar 

  • Conti F., Minelli A., Molnar M., and Brecha N. C. (1994a) Cellular localization and laminar distribution of NMDAR1 mRNA in the rat cerebral cortex.J. Comp. Neurol. 343, 554–565.

    Article  PubMed  CAS  Google Scholar 

  • Conti F., Minelli A., and Brecha N. C. (1994b) Cellular localization and laminar distribution of AMPA glutamate receptor subunits mRNAs and proteins in the rat cerebral cortex.J. Comp. Neurol. 350, 241–259.

    Article  PubMed  CAS  Google Scholar 

  • Conti F., DeBiasi S., Minelli A., and Melone M. (1996) Expression of NR1 and NR2A/B subunits of the NMDA receptor in cortical astrocytes.Glia 17, 254–258.

    Article  PubMed  CAS  Google Scholar 

  • Crick F. (1982) Do dendritic spines twich?Trends Neurosci. 5, 44–46.

    Article  Google Scholar 

  • Currie S. N., Wang X. F., and Daw N. W. (1994) NMDA receptors in layers II and III of rat cerebral cortex.Brain Res. 662, 103–108.

    Article  PubMed  CAS  Google Scholar 

  • DeBiasi S., Minelli, A., Melone M., and Conti F. (1996) Presynaptic NMDA receptors in the neocortex are both auto- and heteroreceptors.NeuroReport, in press.

  • DeFelipe J. and Farinas I. (1992) The pyramidal neurons of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs.Prog. Neurobiol. 39, 563–607.

    Article  PubMed  CAS  Google Scholar 

  • DeFelipe J., Conti F., Van Eyck S. L., and Manzoni T. (1988) Demonstration of glutamate-positive axon terminals forming asymmetric synapses in the cat neocortex.Brain Res. 455, 162–165.

    Article  PubMed  CAS  Google Scholar 

  • Deuchars J., West D. C., and Thomson A. M. (1994) Relationships between morphology and physiology of pyramid-pyramid single axon connections in rat neocortexin vivo.J. Physiol. (Lond.) 478, 423–435.

    Google Scholar 

  • Feldman M. L. (1984) Morphology of the neocortical pyramidal cell, inCerebral Cortex, vol. 1, Cellular Components of the Cerebral Cortex (Peters A. and Jones E. G., eds.), Plenum, New York, pp. 123–200.

    Google Scholar 

  • Forrest D., Yuzaki M., Soares H. D., Ng L., Luk D. C., Sheng M., Stewart C. L., Morgan J. I., Connor J. A., and Curran T. (1994) Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death.Neuron 13, 325–338.

    Article  PubMed  CAS  Google Scholar 

  • Fox K., Sato H., and Daw N. (1989) The location and function of NMDA receptors in cat and kitten visual cortex.J. Neurosci. 9, 2443–2454.

    PubMed  CAS  Google Scholar 

  • Gallo V. and Russell J. T. (1995) Excitatory amino acid receptors in glia: different subtypes for distinct functions?J. Neurosci. Res. 42, 1–8.

    Article  PubMed  CAS  Google Scholar 

  • Gold J. I. and Bear M. F. (1994) A model of dendritic spine Ca2+ concentration exploring possible bases for a sliding synaptic modification threshold.Proc. Natl. Acad. Sci. USA 91, 3941–3945.

    Article  PubMed  CAS  Google Scholar 

  • Greenamyre J. T., Olson J. M. M., Penney J. B., and Young A. B. (1985) Autoradiographic characterization ofN-methyl-d-aspartate-, quisqualate- and kainate-sensitive glutamate binding sites.J. Pharmacol. Exp. Ther. 233, 254–263.

    PubMed  CAS  Google Scholar 

  • Hagihara K., Tsumoto T., Sato H., and Hata Y. (1988) Actions of excitatory amino acid antagonists on geniculo-cortical transmission in the cat's visual cortex.Exp. Brain Res. 69, 407–416.

    Article  PubMed  CAS  Google Scholar 

  • Hollmann M. and Heinemann S. (1994) Cloned glutamate receptors.Ann. Rev. Neurosci. 17, 31–108.

    Article  PubMed  CAS  Google Scholar 

  • Huntley G. W., Vickers J. C., Janssen W., Brose N., Heinemann S. F. and Morrison J. H. (1994) Distribution and synaptic localization of immunocytochemically identified NMDA receptor subunit proteins in sensory-motor and visual cortices of monkey and human.J. Neurosci. 14, 3603–3619.

    PubMed  CAS  Google Scholar 

  • Huntley G. W., Vickers J. C., and Morrison J. H. (1996) Quantitative localization of NMDAR1 receptor subunit immunoreactivity in inferotemporal and prefrontal association cortices of monkey and human. Submitted.

  • Ishii T., Moriyoshi K., Sugihara H., Sakurada K., Kadotani H., Yokoi, M., Akawaza, C., Shigemoto R., Mizuno N., Masu M., and Nakanishi S. (1993) Molecular characterization of the family of theN-methyl-d-aspartate receptor subunits.J. Biol. Chem. 268, 2836–2843.

    PubMed  CAS  Google Scholar 

  • Jaslove S. V. (1992) The integrative properties of spiny distal dendrites.Neuroscience 47, 495–519.

    Article  PubMed  CAS  Google Scholar 

  • Johnson R. R., Jiang X., and Burkhalter A. (1996) Regional and laminar differences in synaptic localization of NMDA receptor subunit NR1 splice variants in rat visual cortex and hippocampus.J. Comp. Neurol. 368, 335–355.

    Article  PubMed  CAS  Google Scholar 

  • Jones E. G. (1993) GABAergic neurons and their role in cortical plasticity.Cereb. Cortex 3 361–372.

    Article  PubMed  CAS  Google Scholar 

  • Jones K. A. and Baughman R. W. (1988) NMDA-and non-NMDA-receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex.J. Neurosci. 8, 3522–3534.

    PubMed  CAS  Google Scholar 

  • Kharazia V. N. and Weinberg R. J. (1994) Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex.J. Neurosci. 14, 6021–6032.

    PubMed  CAS  Google Scholar 

  • Kharazia V. N., Phend K. D., Rustioni A., and Weinberg R. J. (1996) AMPA and NMDA glutamate receptor subunits colocalize at synapses in rat cerebral cortex.Neurosci. Lett. 210, 37–40.

    Article  PubMed  CAS  Google Scholar 

  • Kirchhoff F. and Kettenmann H. (1996) Ionotropic glutamate receptors in vertebrate glial cells, inExcitatory Amino Acids and the Cerebral Cortex. (Conti F. and Hicks, T. P., eds.), MIT Press, Cambridge, MA, pp. 157–166.

    Google Scholar 

  • Kosaka T., Kosaka K., Tateishi K., Hamaoka Y., Yanaihara N., Wu, J.-J., and Hama K. (1985a) GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus.J. Comp. Neurol. 239, 420–430.

    Article  PubMed  CAS  Google Scholar 

  • Kosaka T., Hataguchi Y., Hama K., Nagatsu I., and Wu J.-J. (1985b) Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine.Brain Res. 343, 166–171.

    Article  PubMed  CAS  Google Scholar 

  • Kutsuwada T., Kashiwabuchi N., Mori M., Sakimura K., Kushiya E., Araki K., Meguro H., Masaki H., Kumanishi T., Arakawa M., and Mishina M. (1992) Molecular diversity of the NMDA receptor channel.Nature 358, 36–41.

    Article  PubMed  CAS  Google Scholar 

  • Laurie D. J. and Seeburg P. H. (1994) Regional and developmental heterogeneity in splicing of the rat NMDAR1 mRNA.J. Neurosci. 14, 3180–3194.

    PubMed  CAS  Google Scholar 

  • Laurie D. J., Putzke J., Zieglgansberger W., Seeburg P. H., and Tolle T. R. (1995) The distribution of splice variants of the NMDAR1 subunit mRNA in adult rat brain.Mol. Brain Res. 32, 94–108.

    Article  PubMed  CAS  Google Scholar 

  • LeVay S. (1973) Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi preparations.J. Comp. Neurol. 150, 53–86.

    Article  PubMed  CAS  Google Scholar 

  • Liu, H., Wang H., Sheng M., Jan, L. Y., Jan Y. N., and Basbaum A. I. (1994) Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn.Proc. Natl. Acad. Sci. USA 91, 8383–8387.

    Article  PubMed  CAS  Google Scholar 

  • Maragos W. F., Penney J. B., and Young A. B. (1988) Anatomical correlation of NMDA and [3H]TCP-labelled receptors in rat brain.J. Neurosci. 8, 493–501.

    PubMed  CAS  Google Scholar 

  • McBain C. J. and Mayer M. L. (1994)N-methyl-d-aspartic receptor structure and function.Physiol. Rev. 74, 723–760.

    PubMed  CAS  Google Scholar 

  • Meguro H., Mori H., Araki K., Kushiya E., Kutsuwada T., Yamazaki M., Kumanishi T., Arakawa M., Sakimura K., and Mishina M. (1992) Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs.Nature 357, 70–74.

    Article  PubMed  CAS  Google Scholar 

  • Molinoff P. B., Williams K., Prichett D. B., and Zhong J. (1994) Molecular pharmacology of NMDA receptors: modulatory role of NR2 subunits, inNeuroscience: From the Molecular to the Cognitive, Progress in Brain Research, vol. 100 (Bloom F., ed.), Elsevier, Amsterdam, pp. 39–45.

    Google Scholar 

  • Monaghan D. T. and Cotman C. W. (1985) Distribution ofN-methyl-d-aspartate-sensitivel-[3H] glutamate-binding sites in rat brain.J. Neurosci. 5, 2909–2919.

    PubMed  CAS  Google Scholar 

  • Monaghan D. T., Bridges R. J., and Cotman C. W. (1989) The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system.Ann. Rev. Pharmacol. Toxicol. 29, 365–402.

    Article  CAS  Google Scholar 

  • Monaghan D. T., Holets V. R., Toy D. W., and Cotman C. W. (1983) Anatomical distribution of four pharmacologically distinct [3H]-l-glutamate binding sites.Nature 306, 176–179.

    Article  PubMed  CAS  Google Scholar 

  • Monyer H., Sprengel R., Schoepfer R., Herb A., Higuchi M., Lomeli H., Burnashev N., Sakmann B., and Seeburg P. H. (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes.Science 256, 1217–1221.

    Article  PubMed  CAS  Google Scholar 

  • Monyer H., Burnashev N., Laurie D. J., Sakmann B., and Seeburg P. H. (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors.Neuron 12, 529–540.

    Article  PubMed  CAS  Google Scholar 

  • Mori H. and Mishina M. (1995) Structure and function of the NMDA receptor channel.Neuropharmacology 34 1219–1237.

    Article  PubMed  CAS  Google Scholar 

  • Moriyoshi K., Masu M., Ishii T., Shigemoto R., Mizuno N., and Nakanishi S. (1991) Molecular cloning and characterization of the rat NMDA receptor.Nature 354, 31–37.

    Article  PubMed  CAS  Google Scholar 

  • Nakanishi S. (1992) Molecular diversity of glutamate receptors and implications for brain function.Science 258, 597–603.

    Article  PubMed  CAS  Google Scholar 

  • Parnas H., Parnas I., Ravin R., and Yudelevitch B. (1994) Glutamate and N-methyl-D-aspartate affect release from crayfish axon terminals in a voltage-dependent manner.Proc. Natl. Acad. Sci. USA 91, 11,586–11,590.

    Article  CAS  Google Scholar 

  • Pearce B. (1993) Amino acid receptors, inAstrocytes: Pharmacology and Function (Murphy S., ed.), Academic, San Diego, CA, pp. 47–66.

    Google Scholar 

  • Peters A. (1987) Synaptic specificity in the cerebral cortex, inSynaptic Function (Gall E. and Cowan M., eds.), Wiley, New York, pp. 373–397.

    Google Scholar 

  • Petralia R. S., Yokotani N., and Wenthold R. J. (1994a) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective antipeptide antibody.J. Neurosci. 14, 667–696.

    PubMed  CAS  Google Scholar 

  • Petralia R. S., Wang Y.-X., and Wenthold R. J. (1994b) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1.J. Neurosci. 14, 6102–6120.

    PubMed  CAS  Google Scholar 

  • Rosier A. M., Arckens L., Orban G. A., and Vandesande F. (1993) Laminar distribution of NMDA receptors in cat and monkey visual cortex visualized by [3H]-MK-801 binding.J. Comp. Neurol. 335, 369–380.

    Article  PubMed  CAS  Google Scholar 

  • Saint-Marie R. L. and Peters A. (1985) The morphology and synaptic connections of spiny stellate neurons in monkey visual cortex (area 17): a Golgi-electron microscopic study.J. Comp. Neurol. 233, 213–235.

    Article  PubMed  CAS  Google Scholar 

  • Sheng M., Cummings J., Roldan L. A., Jan Y. N., and Jan L. Y. (1994) Changing subunit composition of heteromeric NMDA receptors during development of rat cortex.Nature 368, 144–147.

    Article  PubMed  CAS  Google Scholar 

  • Sheperd G. M., Woolf T. B., and Carnevale N. T. (1989) Comparisons between active properties of distal dendritic branches and spines: implications for neuronal computations.J. Cogn. Neurosci. 1, 273–286.

    Article  Google Scholar 

  • Sherman A. D., Hegwood T. S., Baruah S., and Waziri R. (1992) Presynaptic modulation of amino acid release from synaptosomes.Neurochem. Res. 17, 125–128.

    Article  PubMed  CAS  Google Scholar 

  • Shirokawa T., Nishigori A., and Kimura F. (1989) Actions of excitatory amino acid antagonists on synaptic potentials of layer II/III neurons of the cat's visual cortex.Exp. Brain Res. 78, 489–500.

    Article  PubMed  CAS  Google Scholar 

  • Siegel S. J., Brose N., Janssen W. G., Gasic G. P., Jahn R., Heinemann S. F., and Morrison J. H. (1994) Regional, cellular, and ultrastructural distribution of the glutamate receptor subunit NMDAR1 in monkey hippocampus.Proc. Natl. Acad. Sci. USA 91, 564–568.

    Article  PubMed  CAS  Google Scholar 

  • Somogyi P. (1978) The study of Golgi stained cells and of experimental degeneration under the electron microscope: a direct method for the identification in the visual cortex of three successive links in a neuron chain.Neuroscience 3, 167–180.

    Article  PubMed  CAS  Google Scholar 

  • Stern P., Béhè P., Schoepfer R., and Colquhoun D. (1992) Single-channel conductances of NMDA receptors expressed from cloned cDNAs: comparison with native receptors.Proc. R. Soc. Lond. B 250, 271–277.

    Article  CAS  Google Scholar 

  • Sucher N. J., Akbarian S., Chi C. L., Leclerc C. L., Awobuluyi M., Deichter D. L., Wu M. K., Yuan J. P., Jones E. G., and Lipton S. A. (1995) Developmental and regional pattern of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain.J. Neurosci. 15, 6509–6520.

    PubMed  CAS  Google Scholar 

  • Thomson A. M. (1986) A magnesium-sensitive postsynaptic potential in rat cerebral cortex resembles neuronal responses toN-methylaspartate.J. Physiol. (Lond.) 370, 531–549.

    CAS  Google Scholar 

  • Thomson A. M. and West D. C. (1993) Fluctuations in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex.Neuroscience 54, 329–346.

    Article  PubMed  CAS  Google Scholar 

  • Thomson A. M. and Deuchars J. (1994) Temporal and spatial properties of local circuits in neocortex.Trends Neurosci. 17, 119–126.

    Article  PubMed  CAS  Google Scholar 

  • Thomson A. M., Deuchars J., and West D. C. (1993) Single axon EPSPs in neocortical interneurones exhibit pronounced paired pulse facilitation.Neuroscience 54, 347–360.

    Article  PubMed  CAS  Google Scholar 

  • Thomson A. M., West D. C., and Deuchars J. (1996) Physiology of glutamatergic transmission in the cerebral cortex, inExcitatory Amino Acids and the Cerebral Cortex (Conti F. and Hicks T. P., eds.), MIT Press, Cambridge, MA, pp. 99–107.

    Google Scholar 

  • Tsumoto T., Masui H., and Sato H. (1986) Excitatory amino acid transmitters in neuronal circuits of the cat visual cortex.J. Neurophysiol. 55, 469–483.

    PubMed  CAS  Google Scholar 

  • Van Bockstaele E. J. and Colago E. E. O. (1996) Selective distribution of the NMDA-R1 glutamate receptor in astrocytes and presynaptic axon terminals in the nucleus locus coeruleus of the rat brain: An immunoelectron microscopic study.J. Comp. Neurol. 369, 483–496.

    Article  PubMed  Google Scholar 

  • Wafford K. A., Bain C. J., Le Bourdelles B., Whiting P. J., and Kemp J. A. (1993) Preferential co-assembly of recombinant NMDA receptors composed of three different subunits.Neuro Report 4, 1347–1349.

    CAS  Google Scholar 

  • Watanabe M., Inoue Y., Sakimura K., and Mishina M. (1993) Distinct distributions of fiveN-methyl-d-aspartate receptor channel subunit mRNAs in the forebrain.J. Comp. Neurol. 338, 377–390.

    Article  PubMed  CAS  Google Scholar 

  • Weinberg R. J. and Kharazia V. N. (1996) Excitatory amino acids in thalamocortical transmission, inExcitatory Amino Acids and the Cerebral Cortex (Conti F. and Hicks T. P., eds.), MIT Press, Cambridge, MA, pp. 109–117.

    Google Scholar 

  • Wenzel A., Scheurer L., Kunzi R., Fritschy J. M., Mohler H., and Benke D. (1995) Distribution of NMDA receptor subunit proteins NR2A, 2B, 2C, and 2D in rat brain.Neuro Report 7, 45–48.

    CAS  Google Scholar 

  • Williams K., Russell, S. L., Shen Y. M., and Molinoff P. B. (1993) Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro.Neuron 10, 267–278.

    Article  PubMed  CAS  Google Scholar 

  • Williams K., Zappia A. M., Pritchett D. B., Shen Y. M., and Molinoff P. B. (1994) Sensitivity of theN-methyl-d-aspartate receptor to polyamine is controlled by NR2 subunits.Mol. Pharmacol. 45, 803–809.

    PubMed  CAS  Google Scholar 

  • Yuste R. and Denk W. (1995) Dendritic spines as basic functional units of neuronal integration.Nature 375, 682–684.

    Article  PubMed  CAS  Google Scholar 

  • Zukin R. S. and Bennett M. V. L. (1995) Alternatively spliced isoforms of the NMDAR1 receptor subunit.Trends Neurosci. 18, 306–313.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Human Physiology, University of Ancona, Ancona, Italy

    Fiorenzo Conti, Andrea Minelli & Marcello Melone

  2. Department of General Physiology and Biochemistry, Section of Histology and Human Anatomy, University of Milan, Milan, Italy

    Silvia DeBiasi

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  1. Fiorenzo Conti
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Conti, F., Minelli, A., DeBiasi, S. et al. Neuronal and glial localization of NMDA receptors in the cerebral cortex. Mol Neurobiol 14, 1–18 (1997). https://doi.org/10.1007/BF02740618

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