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Metabotropic glutamate receptors are associated with non-synaptic appendages of unipolar brush cells in rat cerebellar cortex and cochlear nuclear complex

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Journal of Neurocytology

Abstract

Unipolar brush cells (UBCs) are a class of small neurons that are densely concentrated in the granular layers of the vestibulocerebellar cortex and dorsal cochlear nucleus. The UBCs form giant synapses with individual mossy fibre rosettes on the dendrioles which make up their brush formations and are provided with numerous, unusual non-synaptic appendages. In accord with the glutamatergic nature of mossy fibres, our previous post-embedding immunocytochemical studies indicated that various ionotropic glutamate receptor subunits are localized at the post-synaptic densities of the giant synapses, whereas the non-synaptic appendages are immunonegative. On the contrary, the metabotropic glutamate receptors mGluR1α and mGluR2/3 are situated at the non-synaptic appendages and are lacking at the post-synaptic densities. Other authors, however, have shown that antibodies to these metabotropic receptors stain both appendages and post-synaptic densities. In the present study, we have re-evaluated the distribution of metabotropic glutamate receptors in the UBCs of the cerebellum and the cochlear nuclear complex by light and electron microscopic pre-embedding immunocytochemistry with subtype-specific antibodies. We confirm that UBCs dendritic brushes are densely immunostained by antibody to mGluR1α particularly in the cerebellum and that antibody to mGluR2/3 labels at least a percentage of the UBC brushes in both the cerebellum and cochlear nuclei. At the ultrastructural level, it appears that mGluR1α and mGluR2/3 immunoreactivities are not associated with the post-synaptic densities of the giant mossy fibre–UBC synapses, but instead are concentrated on the non-synaptic appendages of the cerebellar UBCs. The non-synaptic appendages, therefore, may be an important avenue for regulating the excitability of UBCs and mediating glutamate effects on their still unknown intracellular signal transduction cascades. We also show that the pre-synaptic densities of UBC dendrodendritic junctions are mGluR2/3 positive. As previously demonstrated, antibodies to mGluR1 α and mGluR2/3 label subsets of Golgi cells. Antibody to mGluR5 does not stain UBCs in the cerebellum and cochlear nucleus and reveals the somatodendritic compartment of Golgi cells situated in the core of the cerebellar granular layer, whilst cochlear nucleus Golgi cells are mGluR5 negative.

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References

  • Abbott, L. C. & Jacobowitz, D. M. (1995) Development of calretinin-immunoreactive unipolar brush-like cells and an afferent pathway to the embryonic and early postnatal mouse cerebellum. Anatomy and Embryology 191, 541559.

    Google Scholar 

  • Abe, T., Sugihara, H., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1992) Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction. Journal of Biological Chemistry 267, 1336113368.

    Google Scholar 

  • Aiba, A., Kano, M., Chen, C., Stanton, M. E., Fox, G. D., Herrup, K., Zwingman, T. A. & Tonegawa, S. (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79, 377388.

    Google Scholar 

  • Altman, J. & Bayer, S. A. (1977) Time of origin and distribution of a new cell type in the rat cerebellar cortex. Experimental Brain Research 29, 265274.

    Google Scholar 

  • Aniksztejn, L., Otani, S. & Ben-Ari, Y. (1992) Quisqualate metabotropic receptors modulate NMDA currents and facilitate induction of long-term potentiation through protein kinase C. European Journal of Neuroscience 4, 500505.

    Google Scholar 

  • Aoki, E., Semba, R. & Kashiwamata, S. (1986) New candidates for GABAergic neurons in the rat cerebellum: an immunocytochemical study with anti-GABA antibody. Neuroscience Letters 68, 267271.

    Google Scholar 

  • Arai, R., Winsky, L., Arai, M. & Jacobowitz, D. M. (1991) Immunohistochemical localization of calretinin in the rat hindbrain. Journal of Comparative Neurology 310, 2144.

    Google Scholar 

  • Aromori, I. & Nakanishi, S. (1992) Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8, 757765.

    Google Scholar 

  • Baskys, A. (1994) Metabotropic Glutamate Receptors. Austin: Landes, R.G. Comp.

    Google Scholar 

  • Baude, A., Nusser, Z., Roberts, J. D. B., Mulvihill, E., Mcilhinney, J. & Somogyi, P. (1993) The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11, 771787.

    Google Scholar 

  • Berrebi, A. S. & Mugnaini, E. (1991) Distribution and targets of the cartweel axon in the dorsal cochlear nucleus of the guinea pig. Anatomy and Embryology 183, 427454.

    Google Scholar 

  • Berrebi, A. S. & Mugnaini, E. (1993) Alterations in the dorsal cochlear nucleus of cerebellar mutant mice. In The Mammalian Cochlear Nuclei: Organization and Function (edited by MerchÁn, M. A., Juiz, J. M., Godfrey, D. A. & Mugnaini, E.) pp. 107119. New York: Plenum Press.

    Google Scholar 

  • Berrebi, A. S., Morgan, J. I. & Mugnaini, E. (1990) The Purkinje cell class may extend beyond the cerebellum. Journal of Neurocytology 19, 643654.

    Google Scholar 

  • BerthiÉ, B. & Axelrad, H. (1994) Granular layer collaterals of the unipolar brush cell axon display rosette-like excrescences. A Golgi study in the rat cerebellar cortex. Neuroscience Letters 167, 161165.

    Google Scholar 

  • Burry, R. W., VandrÉ, D. D. & Hayes, D. M. (1992) Silver enhancement of gold antibody probes in preembedding electron microscopic immunocytochemistry. Journal of Histochemistry and Cytochemistry 40, 18491856.

    Google Scholar 

  • Cozzi, M. G., Rosa, P., Greco, A., Hille, A., Huttner, W. B., Zanini, A. & de Camilli, P. (1989) Immunohistochemical localization of secretogranin II in the rat cerebellum. Neuroscience 28, 423441.

    Google Scholar 

  • Dunn, M. E., Vetter, D. E., Berrebi, A. S., Krider, H. M. & Mugnaini, E. (1996) The mossy fiber-granule cell-cartwheel cell system in the mammalian cochlear nuclear complex. Advances in Speech, Hearing and Language Processing, 3 (Part A), 6387.

    Google Scholar 

  • Floris, A., DiÑo, M., Jacobowitz, D. M. & Mugnaini, E. (1994) The unipolar brush cells of the rat cerebellar cortex and cochlear nucleus are calretinin-positive: a study by light and electron microscopic immunocytochemistry. Anatomy and Embryology 189, 495520.

    Google Scholar 

  • Fotuhi, M., Sharp, A. H., Glatt, C. E., Hwang, P. M., Von Krosigk, M., Snyder, S. H. & Dawson, T. M. (1993) Differential localization of phosphoinositol-linked metabotropic glutamate receptor (mGluR1) and the inositol 1,4,5-trisphosphate receptor in rat brain. Journal of Neuroscience 13, 20012012.

    Google Scholar 

  • Friedrich, V. L., Jr. & Mugnaini, E. (1981) Preparation of neural tissues for electron microscopy. In Neuro-anatomical Tract-tracing Methods (edited by Heimer, L. & Robards, M. J.) pp. 345375. New York: Plenum.

    Google Scholar 

  • Garthwaite, G. & Garthwaite, J. (1988) Electron microscopic autoradiography of D-[3H]aspartate uptake sites in mouse cerebellar slices shows poor labelling of mossy fibre terminals. Brain Research 343, 129136.

    Google Scholar 

  • Garthwaite, J. & Brodbelt, J. R. (1990) Glutamate as the principal mossy fiber transmitter in rat cerebellum: pharmacological evidence. European Journal of Neuroscience 2, 177180.

    Google Scholar 

  • Glaum, S. R. & Miller, R. J. (1993) Activation of metabotropic receptors produces reciprocal regulation of ionotropic glutamate and GABA responses in the nucleus of the tractus solitarius of the rat. Journal of Neuroscience 13, 16361641.

    Google Scholar 

  • GÖrcs, T. J., Pennke, B., Boti, Z., Katarova, Z. & HÁmori, J. (1993) Immunohistochemical visualization of a metabotropic glutamate receptor. NeuroReport 4, 283286.

    Google Scholar 

  • Grandes, P., Mateos, J. M., Ruegg, D., Kuhn, R. & Knopfel, T. (1994) Differential cellular localization of three splice variants of the mGluR1 metabotropic glutamate receptor in rat cerebellum. NeuroReport 5, 22492252.

    Google Scholar 

  • Hampson, D. R., Theriault, E., Huang, X.-P., Kristensen, P., Pickering, D. S., Franck, J. I. & Mulvihill, E. R. (1994) Characterization of two alternatively spliced forms of a metabotropic glutamate receptor in the central nervous system of the rat. Neuroscience 60, 325336.

    Google Scholar 

  • Harris, J., Moreno, S., Shaw, G. & Mugnaini, E. (1993) Unusual neurofilament composition in cerebellar unipolar brush neurons. Journal of Neurocytology 22, 663681.

    Google Scholar 

  • Hayashi, Y., Momiyama, A., Takahashi, T., Ohishi, H., Ogawa-Meguro, R., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993) Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb. Nature 366, 687690.

    Google Scholar 

  • Hockfield, S. (1987) A Mab to a unique cerebellar neuron generated by immunosuppression and rapid immunization. Science 237, 6770.

    Google Scholar 

  • Hollman, M. & Heinemann, S. (1994) Cloned glutamate receptors. Annual Review of Neuroscience 17, 31108.

    Google Scholar 

  • Ito, M. (1984) The Cerebellum and Neural Control. New York: Raven.

    Google Scholar 

  • Jaarsma, D., Wenthold, R. & Mugnaini, E. (1995) Glutamate receptor subunits at mossy fibre-unipolar brush cell synapses: light and electron microscopic immunocytochemical study in cerebellar cortex of rat and cat. Journal of Comparative Neurology 357, 145160.

    Google Scholar 

  • Jaarsma, D., DiÑo, M. R., Cozzari, C. & Mugnaini, E. (1997a) Cerebellar choline acetyltransferase positive mossy fibres and their granule and unipolar brush cell targets: a model for central cholinergic nicotinic neurotransmission. Journal of Neurocytology 25, 829842.

    Google Scholar 

  • Jaarsma, D., Ruigrok, T. J. H., CaffÉ, R., Cozzari, C., Levey, A. I., Mugnaini, E. & Voogd, J. (1997b) Cholinergic innervation and receptors in the cerebellum. Progress in Brain Research 114, 6796.

    Google Scholar 

  • Ji, Z., Aas, J.-E., Laake, J., Walberg, F. & Ottersen, P. O. (1991) An electron microscopic, immunogold analysis of glutamate and glutamine in terminals of rat spinocerebellar fibres. The Journal of Comparative Neurology 307, 296310.

    Google Scholar 

  • Kaupmann, K., Huggel, K., Heid, J., Flor, P. J., Bischoff, S., Mickel, S. J., Mcmaster, G., Angst, C., Bittiger, H., Froestl, W. & Bettler, B. (1997) Expression cloning of GABAB receptors uncovers similarity to metabotropic glutamate receptors. Nature 386, 239246.

    Google Scholar 

  • Kristensen, P., Suzdak, P. D. & Thomsen, C. (1993) Expression pattern and pharmacology of the rat type IV metabotropic glutamate receptor. Neuroscience Letters 155, 159162.

    Google Scholar 

  • Laurie, D. J., Boddeke, H. W. G. M., Hiltscher, R. & Sommer, B. (1996) HmGlu1d, a novel splice variant of the human type I metabotropic glutamate receptor. European Journal of Pharmacology 296, R1R3.

    Google Scholar 

  • Lujan, R., Roberts, J. D., Shigemoto, R., Ohishi, H. & Somogyi, P. (1997) Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1 alpha, mgluR2 and mGluR5, relative to neurotransmitter release sites. Journal of Chemical Neuroanatomy 13, 219241.

    Google Scholar 

  • Martin, L. J., Blackstone, C. D., Huganir, R. L. & Price, D. L. (1992) Cellular localisation of a metabotropic glutamate receptor in rat brain. Neuron 9, 259270.

    Google Scholar 

  • Miles, F. A. & Braitman, D. J. (1980) Long-term adaptive changes in the primate vestibulocular reflex. II Electrophysiological observations on semicircular canal primary afferents. Journal of Neurophysiology 43, 14261436.

    Google Scholar 

  • Mugnaini, E. & Floris, A. (1994) The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex. Journal of Comparative Neurology 339, 174180.

    Google Scholar 

  • Mugnaini, E., Osen, K. K., Dahl, A.-L., Friedrich, V. L., Jr & Korte, G. (1980a) Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse. Journal of Neurocytology 9, 537570.

    Google Scholar 

  • Mugnaini, E., Warr, W. B. & Osen, K. K. (1980b) Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat and mouse. Journal of Comparative Neurology 191, 581606.

    Google Scholar 

  • Mugnaini, E., Floris, A. & Wright-Goss, M. (1994) Extraordinary synapses of the unipolar brush cell: an electron microscopic study in the rat cerebellum. Synapse 16, 284311.

    Google Scholar 

  • Mugnaini, E., DiÑo, M. R. & Jaarsma, D. (1997) The unipolar brush cells of the mammalian cerebellum and cochlear nucleus: cytology and microcircuitry. Progress in Brain Research, 114, 131150.

    Google Scholar 

  • Nakanishi, S. (1994) Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron 13, 10311037.

    Google Scholar 

  • Neki, A., Ohishi, H., Kaneko, T., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1996) Metabotropic glutamate receptors mGluR2 and mGluR5 are expressed in two non-overlapping populations of Golgi cells in the rat cerebellum. Neuroscience 75, 815826.

    Google Scholar 

  • Nusser, Z., Mulvihill, E., Streit, P. & Somogyi, P. (1994) Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61, 421427.

    Google Scholar 

  • O’Connor, J. J., Rowan, M. J. & Anwyl, R. (1994) Long-lasting enhancement of NMDA receptormediated synaptic transmission by metabotropic glutamate receptor activation. Nature 367, 227229.

    Google Scholar 

  • Ohishi, H., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1993a) Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience 53, 10091018.

    Google Scholar 

  • Ohishi, H., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1993b) Distribution of the messenger RNA for a metabotropic glutamate receptor (mGluR2) in the rat brain: an in situ hybridisation study. Journal of Comparative Neurology 335, 252266.

    Google Scholar 

  • Ohishi, H., Ogawa-Meguro, R., Shigemoto, R., Kaneko, T., Nakanishi, S. & Mizuno, N. (1994) Immunohistochemical localization of metabotropic glutamate receptors, mGluR2 and mGluR3, in rat cerebellar cortex. Neuron 13, 5566.

    Google Scholar 

  • Ohishi, H., Akazawa, C., Shigemoto, R., Nakanishi, S. & Mizuno, N. (1995) Distributions of the mRNAs for l-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. Journal of Comparative Neurology 360, 555570.

    Google Scholar 

  • Ohishi, H., Neki, A. & Mizuno, N. (1998) Distribution of a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat and mouse: an immunocytochemical study with a monoclonal antibody. Neuroscience Research 30, 6582.

    Google Scholar 

  • Okamoto, N., Hori, S., Akazawa, C., Hayashi, Y., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1994) Molecular characterization of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. Journal of Biological Chemistry 269, 12311236.

    Google Scholar 

  • Ottersen, O. P. & Landsend, A. S. (1997) Organization of glutamate receptors at the synapse. European Journal of Neuroscience 9, 22192224.

    Google Scholar 

  • Ottersen, O. P., Laake, J. H. & Storm-Mathisen, J. (1990) Demonstration of a releasable pool of glutamate in cerebellar mossy and parallel fibre terminals by means of light and electron microscopic immunocytochemistry. Archives Italiennes de Biologie 128, 111125.

    Google Scholar 

  • Persechini, A., Moncrief, N. D. & Krestinger, R. H. (1989) The EF-hand family of calcium-modulated proteins. Trends in Neuroscience 12, 462467.

    Google Scholar 

  • Petralia, R. S., Wang, Y.-X., Zhao, H.-M. & Wenthold, R. J. (1996a) Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. Journal of Comparative Neurology 372, 356383.

    Google Scholar 

  • Petralia, R. S., Wang, Y.-X., Niedzielski, A. S. & Wenthold, R. J. (1996b) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71, 949976.

    Google Scholar 

  • Petralia, R. S., Wang, Y.-X., Singh, S., Wu, C., Shi, L., Wei, J. & Wenthold, R. J. (1997) A monoclonal antibody shows discrete cellular and subcellular localizations of mGluR1α metabotropic glutamate receptors. Journal of Chemical Neuroanatomy 13, 7793.

    Google Scholar 

  • Pin, J. P. & Duvoisin, R. (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34, 126.

    Google Scholar 

  • Pin, J. P., Waeber, C., Prezeau, L., Bockaert, J. & Heineman, S. F. (1992) Alternative splicing generates metabotropic glutamate receptors inducing different patterns of calcium release in Xenopous oocytes. Proceedings of the National Academy of Sciences USA 89, 1033110335.

    Google Scholar 

  • RÉsibois, A. & Rogers, J. H. (1992) Calretinin in rat brain: an immunohistochemical study. Neuroscience 46, 101134.

    Google Scholar 

  • Roche, K.W., Tingley, W. G. & Huganir, R. L. (1994) Glutamate receptor phosphorylation and synaptic plasticity. Current Opinion in Neurobiology 4, 383388.

    Google Scholar 

  • Rogers, J. H. (1989) Immunoreactivity for calretinin and other calcium-binding proteins in cerebellum. Neuroscience 31, 711721.

    Google Scholar 

  • Rossi, R. J., Mugnaini, E. & Slater, N. T. (1994) Glutamate receptor-mediated transmission at a novel giant synapse in rat cerebellum; the mossy fibre-unipolar brush cell synapse. Brain Research Association Abstracts 11, 29.

    Google Scholar 

  • Rossi, R. J., Alford, S. T., Mugnaini, E. & Slater, N. T. (1995) Time course of transmission at a giant glutamatergic synapse in cerebellum, the mossy fiber-unipolar brush cell synapse. Journal of Neurophysiology 74, 2442.

    Google Scholar 

  • Saugstad, J. A., Kinzie, J. M., Mulvihill, E. R., Segerson, T. P. & Westbrok, G. L. (1994) Cloning and expression of a new member of the L-AP4-sensitive class of metabotropic glutamate receptors. Molecular Pharmacology 45, 363367.

    Google Scholar 

  • Schoepp, D. D. (1994) Novel functions for subtypes of metabotropic glutamate receptors. Neurochemistry International 24, 439449.

    Google Scholar 

  • Schuerger, R. J., DiÑo, M. R., Liu, Y.-B., Slater, N. T. & Mugnaini, E. (1997) Light and electron microscopic identification of the axon terminals and post-synaptic targets of cerebellar unipolar brush cells. Society for Neuroscience Abstracts 23, 712.13

    Google Scholar 

  • Sekerkova, G. & Mugnaini, E. (1997) Prenatal neurogenesis of cerebellar unipolar brush cells studied by bromodeoxyuridine and cell class specific markers. Society for Neuroscience Abstracts 23, 712.15.

    Google Scholar 

  • Shigemoto, R., Nakanishi, S. & Mizuno, N. (1992) Distribution of mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: an in situ hybridisation study in adult and developing rat. Journal of Comparative Neurology 322, 121135.

    Google Scholar 

  • Shigemoto, R., Nomura, S., Ohishi, H., Sugihara, H., Nakanishi, S. & Mizuno, N. (1993) Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neuroscience Letters 163, 5357.

    Google Scholar 

  • Shigemoto, R., Abe, T., Nomura, S., Nakanishi, S. & Hirano, T. (1994) Antibodies inactivating mGluR1 metabotropic glutamate receptor block long-term depression in cultured Purkinje cells. Neuron 12, 12451255.

    Google Scholar 

  • Shigemoto, R., Kulik, A., Roberts, J. D., Ohishi, H., Nusser, Z., Kaneko, T. & Somogyi, P. (1996) Target cell specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381, 523525.

    Google Scholar 

  • Shigemoto, R., Kinoshita, A., Wada, E., Nomura, S., Ohishi, H., Takada, M., Flor, P. J., Neki, A., Abe, T., Nakanishi, S. & Mizuno, N. (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. Journal of Neuroscience 17, 75037522.

    Google Scholar 

  • Silver, R. A., Traynelis, S. F. & Cull-Candy, S. G. (1992) Rapid-time course miniature and evoked excitatory current at cerebellar synapses in situ. Nature 355, 163166.

    Google Scholar 

  • Slater, N. T., Rossi, D. J. & Kinney, G. A. (1997) Physiology of transmission at a giant glutamatergic synapse in the cerebellum. Progress in Brain Research 114, 151163.

    Google Scholar 

  • Slater, N. T., Rossi, D. J., DiÑo, M. R., Jaarsma, D. & Mugnaini, E. (1998) Physiology and ultrastructure of unipolar brush cells in the vestibulocerebellum. In Neurochemistry of the Vestibular System (edited by Betz, A. & Andersen, J.) Orlando,FL: CRC press, Inc., in press.

    Google Scholar 

  • Somogyi, P., Halashy, K. Somogyi, J., Stormmathisen, J. & Ottersen, O. P. (1986) Quantitation of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience 19, 10451050.

    Google Scholar 

  • Takahashi, T., Forsythe, I. D., Tsujimoto, T., Barnes-Davies, M. & Onodera, K. (1996) Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274, 594597.

    Google Scholar 

  • Tanabe, Y., Masu, M., Ishii, T., Shigemoto, R. & Nakanishi S. (1992) A family of metabotropic glutamate receptors. Neuron 8, 169179.

    Google Scholar 

  • Tanabe, Y., Nomura, A., Masu, M., Shigemoto, R., Mizuno, N. & Nakanishi, S. (1993) Signal transduction, pharmacological properties, and expression patterns of two metabotropic glutamate receptors, mGluR3 and mGluR4. Journal of Neuroscience 13, 13721378.

    Google Scholar 

  • Weedman, D. L., Pongstaporn, T. & Ryugo, D. K. (1996) Ultrastructural study of the granule cell domain of the cochlear nucleus in rats: mossy fiber endings and their targets. Journal of Comparative Neurology 369, 345360.

    Google Scholar 

  • Wright, D. D. & Ryugo, D. K. (1995) Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. Journal of Comparative Neurology 365, 159172.

    Google Scholar 

  • Wright, D. D., Blackstone, C. D., Huganir, R. L. & Ryugo, D. K. (1996) Immunocytochemical localization of the mGluR1α metabotropic glutamate receptor in the dorsal cochlear nucleus. Journal of Comparative Neurology 364, 729745.

    Google Scholar 

  • Yokoi, M., Kobayashi, K., Manabe, T., Takahashi, T., Sakaguchi, I., Katsuura, G., Shigemoto, R., Ohishi, H., Nomura, S., Nakamura, K., Nakao, K., Katsuki, M. & Nakanishi, S. (1996) Impairment of hippocampal mossy fiber LTD in mice lacking mGluR2. Science 273, 645647.

    Google Scholar 

  • Zirpel, L., Lachica, E. A. & Rubel, E. W. (1995) Activation of a metabotropic glutamate receptor increases intracellular calcium concentrations in neurons of the avian cochlear nucleus. Journal of Neuroscience 15, 214222.

    Google Scholar 

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Jaarsma, D., Dino, M.R., Ohishi, H. et al. Metabotropic glutamate receptors are associated with non-synaptic appendages of unipolar brush cells in rat cerebellar cortex and cochlear nuclear complex. J Neurocytol 27, 303–327 (1998). https://doi.org/10.1023/A:1006982023657

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