Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus

Journal of Comparative Neurology

Volumn 372, Issue 3, 1996, Pages 356-383

  Petralia, Ronald S ^a   Wang, Ya Xian ^a   Zhao, Hui Min ^a   Wenthold, Robert J ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

AMPA; auditory; delta; kainate; NMDA

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMIC ACID; KAINIC ACID; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; BRUSH BORDER; CEREBELLUM; COCHLEAR NUCLEUS; GLIA; GRANULE CELL; IMMUNOCYTOCHEMISTRY; INTERNEURON; MALE; MOSSY FIBER; NEUROANATOMY; NEUROPIL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SPINDLE CELL; SYNAPSE;

EID: 0029826840     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(sici)1096-9861(19960826)372:3<356::aid-cne3>3.3.co;2-%23     Document Type: Article

References (117)

1. Adams, J.C. (1979) Ascending projections to the inferior colliculus. J. Comp. Neurol. 183:519-538.
2. Adams, J.C. and W.B. Warr (1976) Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts. J. Comp. Neurol. 170:107-122.
3. Berrebi, A.S. and E. Mugnaini (1991) Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat. Embryol. 183:427-454.
4. Brawer, J.B., D.K. Morest, and E.C. Kane (1974) The neuronal architecture of the cochlear nucleus of the cat. J. Comp. Neurol. 155:251-300.
5. Cant, N.B. (1992) The cochlear nucleus: Neuronal types and their synaptic organization. In D.B. Webster, A.N. Popper, and R.R. Fay (eds): The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, pp. 66-116.
6. Caspary, D.M. (1986) Cochlear nuclei: Functional neuropharmacology of the principal cell types. In R A. Altschuler, D.W. Hoffman, and R.P. Bobbin (eds): Neurobiology of Hearing: The Cochlea. New York: Raven, pp. 303-332.
7. Chen, B. and R.G. Pourcho (1995) Morphological diversity and glutamate immunoreactivity of retinal terminals in the suprachiasmatic nucleus of the cat. J. Comp. Neurol. 361:108-118.
8. Coombs, S.L., J.C. Montgomery, and R.A. Conley (1994) A comparative overview of brainstem organization and function in octavolateralis systems. Assoc. Res. Otolaryngol. Abs. 17:155.
9. Floris, A., M. Dino, D.M. Jacobowitz, and E. Mugnaini (1994) The unipolar brush cells of the rat cerebellar cortex and cochlear nucleus are calretinin-positive: A study by light and electron microscopic immunocytochemistry. Anat. Embryol. 189:495-520.
10. Francis, H.W. and P.B. Manis (1995) Antagonism of phorbol ester stimulation of protein kinase C by bisindolylmaleimide and calphostin C in the molecular layer of the dorsal cochlear nucleus. Assoc. Res. Otolaryngol. Abs. 18:38.
11. 28k in the auditory system of adult and developing rats. J. Comp. Neurol. 349:193-211.
12. Furuyama, T., H. Kiyama, K. Sato, H.T. Park, H. Maeno, H. Takagi, and M. Tohyama (1993) Region-specific expression of subunits of ionotropic glutamate receptors (AMPA-type, KA-type and NMDA receptors) in the rat spinal cord with special reference to nociception. Mol. Brain Res. 18:141-151.
13. Gallo, V., L.M. Upson, W.P. Hayes, L. Vyklicky, C.A. Winters, and A. Buonanno (1992) Molecular cloning and developmental analysis of a new glutamate receptor subunit isoform in cerebellum. J. Neurosci. 12:1010-1023.
14. Garcia, M.M., C.G. Cusick, and R.E. Harlan (1993) Protein kinase C-delta in rat brain: Association with sensory neuronal hierarchies. J. Comp. Neurol. 331:375-388.
15. 2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15:193-204.
16. 3H) glutamate-binding sites in rat central nervous system. J. Neurosci. 4:2133-2144.
17. Hackney, C.M., K.K. Osen, and J. Kolston (1990) Anatomy of the cochlear nuclear complex of guinea pig. Anat. Embryol. 182:123-149.
18. Halpain, S., C.M. Wieczorek, and T.C. Rainbow (1984) Localization of L-glutamate receptors in rat brain by quantitative autoradiography. J. Neurosci. 4:2247-2258.
19. Harrison, J.M. and W.B. Warr (1962) A study of the cochlear nuclei and ascending auditory pathways of the medulla. J. Comp. Neurol. 119:341-379.
20. Hámori, J., J. Takacs, and P. Petrusz (1990) Immunogold electron microscopic demonstration of glutamate and GABA in normal and deafferented cerebellar cortex: Correlation between transmitter content and synaptic vesicle size. J. Histochem. Cytochem. 38:1767-1777.
21. Helfert, R.H., C.R. Snead, and R.A. Altschuler (1991) The ascending auditory pathways. In R.A. Altschuler, R.P. Bobbin, B.M. Clopton and D.W. Hoffman (eds): Neurobiology of Hearing: The Central Auditory System. New York: Raven, pp. 1-25.
22. Hirano, T., K. Kasono, K. Araki, K. Shinozuka, and M. Mishina (1994) Involvement of the glutamate receptor δ2 subunit in the long-term depression of glutamate responsiveness in cultured rat Purkinje cells. Neurosci. Lett. 182:172-176.
23. Hunter, C., R.S. Petralia, T. Vu, and R.J. Wenthold (1993) Expression of AMPA-selective glutamate receptor subunits in morphologically defined neurons of the mammalian cochlear nucleus. J. Neurosci. 13:1932-1946.
24. Hunter, C. and R.J. Wenthold (1994) Overlapping expression patterns for kainate-, NMDA- and AMPA-selective glutamate receptor subunit mRNAs in the rat cochlear nucleus. Assoc. Res. Otolaryngol. Abs. 17:14.
25. Huntley, G.W., S.W. Rogers, T. Moran, W. Janssen, N. Archin, J.C. Vickers, K. Cauley, S.F. Heinemann, and J.H. Morrison (1993) Selective distribution of kainate receptor subunit immunoreactivity in monkey neocortex revealed by a monoclonal antibody that recognizes glutamate receptor subunits GluR5/6/7. J. Neurosci. 13:2965-2981.
26. Hutson, K.A. and D.K. Morest (1994) Ultrastructure of small cell regions in the cochlear nucleus (CN) of chinchilla. Assoc. Res. Otolaryngol. Abs. 17:27.
27. Jaarsma, D., R.J. Wenthold, and E. Mugnaini (1995) Glutamate receptor subunits at mossy fiber-unipolar brush cell synapses: Light and electron microscopic immunocytochemical study in cerebellar cortex of rat and cat. J. Comp. Neurol. 357:145-160.
28. 2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12:1281-1289.
29. Kaltenbach, J.A., R.J. Meleca, P.R. Falzarano, S.F. Myers, and T.H. Simpson (1993) Forward masking properties of neurons in the dorsal cochlear nucleus: Possible role in the process of echo suppression. Hear. Res. 67:35-44.
30. Kaltenbach, J.A. and D. McCaslin (1995) A circuit model for the process of echo suppression linking the dorsal cochlear nucleus with cochlear outer hair cells. Assoc. Res. Otolaryngol. Abs. 18:133.
31. Kane, E.S., S.G. Puglisi, and B.S. Gordon (1981) Neuronal types in the deep dorsal cochlear nucleus of the cat: I. Giant neurons. J. Comp. Neurol. 198:483-513.
32. Kashiwabuchi, N., K. Ikeda, K. Araki, T. Hirano, K. Shibuki, C. Takayama, Y. Inoue, T. Kutsuwada, T. Yagi, Y. Kang, S. Aizawa, and M. Mishina (1995) Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluRδ2 mutant mice. Cell 81:245-252.
33. Keinänen, K., W. Wisden, B. Sommer, P. Werner, A. Herb, T.A. Verdoorn, B. Sakmann, and P.H. Seeburg (1990) A family of AMPA-selective glutamate receptors. Science 249:556-560.
34. Kolston, J., K.K. Osen, C.M. Hackney, O.P. Ottersen and J. Storm-Mathisen (1992) An atlas of glycine- and GABA-like immunoreactivity in the cochlear nuclear complex of the guinea pig. Anat. Embryol. 186:443-465.
35. Lachica, E.A., R. Rübsamen, L. Zirpel, and E.W. Rubel (1995) Glutamatergic inhibition of voltage-operated calcium channels in the avian cochlear nucleus. J. Neurosci. 15:1724-1734.
36. Linden, D.J. (1994) Long-term synaptic depression in the mammalian brain. Neuron 12:457-472.
37. Manis, P.B. (1989) Responses to parallel fiber stimulation in the guinea pig dorsal cochlear nucleus in vitro. J. Neurophysiol. 61:149-161.
38. Manis, P.B., G.A. Spirou, D.D. Wright, S. Paydar, and D.K. Ryugo (1994) Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J. Comp. Neurol. 348:261-276.
39. Martin, L.J., C.D. Blackstone, R.L. Huganir, and D.L. Price (1992) Cellular localization of a metabotropic glutamate receptor in the rat brain. Neuron 9:259-270.
40. Martin, L.J., C.D. Blackstone, A.I. Levey, R.L. Huganir, and D.L. Price (1993) AMPA glutamate receptor subunits are differentially distributed in rat brain. Neuroscience 53:327-358.
41. Mayat, E., R.S. Petralia, Y.-X. Wang, and R.J. Wenthold (1995) Immunoprecipitation, immunoblotting and immunocytochemistry studies suggest that glutamate receptor delta subunits form novel postsynaptic receptor complexes. J. Neurosci. 15:2533-2546.
42. 3H] kainic acid binding sites in rat CNS as determined by autoradiography. Brain Res. 252:91-100.
43. 3H]glutamate-binding sites in rat brain. J. Neurosci. 5:2909-2919.
44. Mosbacher, J., R. Schoepfer, H. Monyer, N. Burnashev, P.H. Seeburg, and J.P. Ruppersberg (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266:1059-1062.
45. Mugnaini, E., K.K. Osen, A.-L. Dahl, V.L. Friedrich, and G. Korte (1980a) Fine structure of granule cells and related interneurons (termed Golgi cells) in the cochlear nuclear complex of cat, rat and mouse. J. Neurocytol. 9:537-570.
46. Mugnaini, E., W.B. Warr, and K.K. Osen (1980b) Distribution and light microscopic features of granule cells in the cochlear nuclei of cat, rat, and mouse. J. Comp. Neurol. 191:581-606.
47. Mugnaini, E. (1985) GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: Light and electron microscopic immunocytochemistry. J. Comp. Neurol. 235:61-81.
48. Mugnaini, E. and J.I. Morgan (1987) The neuropeptide cerebellin is a marker for two similar neuronal circuits in rat brain. Proc. Natl. Acad. Sci. USA 84:8692-8696.
49. Mugnaini, E. and A. Floris (1994) The unipolar brush cell: A neglected neuron of the mammalian cerebellar cortex. J. Comp. Neurol. 339:174-180.
50. Mugnaini, E., A. Floris, and M. Wright-Goss (1994) Extraordinary synapses of the unipolar brush cell: An electron microscopic study in the rat cerebellum. Synapse 16:284-311.
51. Müller, T., T. Möller, T. Berger, J. Schnitzer, and H. Kettenmann (1992) Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells. Science 256:1563-1566.
52. Nakanishi, S. (1994) Metabotropic glutamate receptors: Synaptic transmission, modulation, and plasticity. Neuron 13:1031-1037.
53. Ohishi, H., R. Shigemoto, S. Nakanishi, and N. Mizuno (1993a) Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience 53:1009-1018.
54. Ohishi, H., R. Shigemoto, S. Nakanishi, and N. Mizuno (1993b) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: An in situ hybridization study. J. Comp. Neurol. 335:252-266.
55. Ohishi, H., R. Ogawa-Meguro, R. Shigemoto, S. Nakanishi, and N. Mizuno (1994) Immunohistochemical localization of metabotropic glutamate receptors, mGluR2 and mGluR3, in rat cerebellar cortex. Neuron 13:55-66.
56. Osen, K.K., O.P. Ottersen, and J. Storm-Mathisen (1990) Colocalization of glycine-like and GABA-like immunoreactivities: A semiquantitative study of individual neurons in the dorsal cochlear nucleus of cat. In O.P. Ottersen and J. Storm-Mathisen (eds): Glycine Neurotransmission. New York: John Wiley & Sons Ltd, pp. 417-451.
57. Osen, K.K., J. Storm-Mathisen, O.P. Ottersen, and B. Dihle (1995) Glutamate is concentrated in and released from parallel fiber terminals in the dorsal cochlear nucleus: A quantitative immunocytochemical analysis in guinea pig. J. Comp. Neurol. 357:482-500.
58. Palombi, P.S., P.M. Backoff, and D.M. Caspary (1994) Paired tone facilitation in dorsal cochlear nucleus neurons: A short-term potentiation model testable in vivo. Hear. Res. 75:175-183.
59. Paxinos, G. and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates. New York: Academic Press.
60. Petralia, R.S. (1996) Immunocytochemical localization of ionotropic glutamate receptors in neural circuits. In D.T. Monaghan and R.J. Wenthold (eds): The Ionotropic Glutamate Receptors. Totowa, N.J.: Humana Press. (in press).
61. Petralia, R.S. and R.J. Wenthold (1992a) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318:329-354.
62. Petralia, R.S. and R.J. Wenthold (1992b) Localization of AMPA-selective glutamate receptor subunits in the cochlear nuclei of the rat using characterized antipeptide antibodies. Assoc. Res. Otolaryngol. Abs. 15:20.
63. Petralia, R.S. and R.J. Wenthold (1992c) Light and electron microscopic localization of AMPA-selective glutamate receptors in the cochlear nuclei of the rat using subunit-specinc antipeptide antibodies. Molec. Biol. Hear. Deafness:106.
64. Petralia, R.S. and R.J. Wenthold (1993) Localization of metabotropic glutamate receptor subunit (mGluR1α) in the cochlear nuclei of the rat using a selective antipeptide antibody. Funct. Neurol. 8, Suppl N. 4:41.
65. Petralia, R.S. and R.J. Wenthold (1995) Types of excitatory amino acid receptors and their localization in the nervous system and hypothalamus. In D.W. Brann and V.B. Mahesh (eds): Excitatory Amino Acids: Their Role in Neuroendocrine Function. Boca Raton, Florida: CRC Press, pp. 55-101.
66. Petralia, R.S., N. Yokotani, and R.J. Wenthold (1994a) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14:667-696.
67. Petralia, R.S., Y.-X. Wang, and R.J. Wenthold (1994b) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J. Neurosci. 14:6102-6120.
68. Petralia, R.S., Y.-X. Wang, and R.J. Wenthold (1994c) Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349:85-110.
69. Petralia, R.S., Y.-X. Wang, and R.J. Wenthold (1994d) Comparative distribution of glutamate receptor subunits in the cochlear nuclei of the rat using characterized antipeptide antibodies. Assoc. Res. Otolaryngol. Abs. 17:14.
70. Petralia, R.S., Y.-X. Wang, and R.J. Wenthold (1995a) Distribution of the glutamate receptor subunits delta 1&2 and mGluR2&3 in the cochlear nuclei using two characterized antipeptide antibodies. Assoc. Res. Otolaryngol. Abs. 18:31.
71. Petralia, R.S., V.A. Trumpy, N.S. Alvanzo, and R.J. Wenthold (1993) Localization of kainate (KA2) and metabotropic (mGluR1α) glutamate receptors in the cochlear nuclei of the rat using characterized antipeptide antibodies Assoc. Res. Otolaryngol. Abs. 16:120.
72. Petralia, R.S., Y.-X. Wang, H.-M. Zhao, and R.J. Wenthold (1995b) Comparative distribution of ionotropic and metabotropic glutamate receptors in the dorsal cochlear nucleus. Molec. Biol. Hear. Deafness:123.
73. Petralia, R.S., Y.-X. Wang, A.S. Niedzielski, and R.J. Wenthold (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71:949-976.
74. Pin, J.-P. and R. Duvoisin (1995) The metabotropic glutamate receptors: Structure and functions. Neuropharmacology 34:1-26.
75. Raman, I.M., S. Zhang, and L.O. Trussell (1994) Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling. J. Neurosci. 14:4998-5010.
76. Résibois, A. and J.H. Rogers (1992) Calretinin in rat brain: An immunohistochemical study. Neuroscience 46:101-134.
77. Rodrigo, J., O. Uttenthal, M.L. Bentura, N. Maeda, K. Mikoshiba, R. Martinez-Murillo, and J.M. Polak (1994) Subcellular localization of the inositol 1,4,5-trisphosphate receptor, P400, in the vestibular complex and dorsal cochlear nucleus of the rat. Brain Res. 634:191-202.
78. 28k in rat brain: Patterns of partial co-localization. Neuroscience 51:843-865.
79. Romano, C., M.A. Sesma, C. MacDonald, K. O'Malley, A.N. van den Pol, and J.W. Olney (1995) Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J. Comp. Neurol. 355:455-469.
80. Rubio, M.E. (1994) Distribución Sináptica de Neurotransmisores Excitatorios e Inhibitorios en un Núcleo Auditivo. Doctoral Thesis. Spain: University of Alicante, Institute of Neurosciences.
81. Rubio, M.E., P.B. Manis, and R.J. Wenthold (1996) Targeting of glutamate receptor subunits to synaptic populations of fusiform cells of the DCN. Assoc. Res. Otolaryngol. Abs. 19:167.
82. Ryugo, D.K. (1992) The auditory nerve: Peripheral innervation, cell body morphology, and central projections. In D.B. Webster, A.N. Popper, and R.R. Fay (eds): The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, pp. 23-65.
83. Ryugo, D.K., T. Pongstaporn, D.D. Wright, and A.H. Sharp (1995) Inositol 1,4,5-trisphosphate receptors: Immunocytochemical localization in the dorsal cochlear nucleus. J. Comp. Neurol. 358:102-118.
84. Saito, N., U. Kikkawa, Y. Nishizuka, and C. Tanaka (1988) Distribution of protein kinase C-like immunoreactive neurons in rat brain. J. Neurosci. 8:369-382.
85. Schwartz, I.R. (1994) Immunocytochemistry of glutamate receptor subunits in the gerbil cochlear nucleus and superior olivary complex. Assoc. Res. Otolaryngol. Abs. 17:14.
86. Schwartz, I.R. and P.R. Eager (1995) Ultrastructural localization of glutamate receptor subunit immunoreactivity in the cochlear nucleus and superior olivary complex. Assoc. Res. Otolaryngol. Abs. 18:39.
87. Shigemoto, R., S. Nakanishi, and N. Mizuno (1992) Distribution of the mRNA for a metabotropic glutamate receptor (mGluR1) in the central nervous system: An in situ hybridization study in adult and developing rat. J. Comp. Neurol. 322:121-135.
88. Siegel, S.J., N. Brose, W.G. Janssen, G.P. Gasic, R. Jahn, S.F. Heinemann, and J.H. Morrison (1994) Regional, cellular, and ultrastructural distribution of N-methyl-D-aspartate receptor subunit 1 in monkey hippocampus. Proc. Natl. Acad. Sci. USA 91:564-568.
89. Smith, P.H. and W.S. Rhode (1985) Electron microscopic features of physiologically characterized, HRP-labeled fusiform cells in the cat dorsal cochlear nucleus. J. Comp. Neurol. 237:127-143.
90. Sucher, N.J., N. Brose, D.L. Deitcher, M. Awobuluyi, G.P. Gasic, H. Bading, C.L. Cepko, M.E. Greenberg, R. Jahn, S.F. Heinemann, and S.A. Lipton (1993) Expression of endogenous NMDAR1 transcripts without receptor protein suggests post-transcriptional control in PC12 cells. J. Biol. Chem. 268:22299-22304.
91. Tachibana, M., R.J. Wenthold, H. Morioka, and R.S. Petralia (1994) Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat spinal cord. J. Comp. Neurol. 344:431-454.
92. Takayama, C., S. Nakagawa, M. Watanabe, M. Mishina, and Y. Inoue (1995) Light- and electron-microscopic localization of the glutamate receptor channel δ2 subunit in the mouse Purkinje cell. Neurosci. Lett. 188:89-92.
93. van den Pol, A.N. (1995) Presynaptic metabotropic glutamate receptors in adult and developing neurons: Autoexcitation in the olfactory bulb. J. Comp. Neurol. 359:253-271.
94. Watanabe, M., M. Mishina, and Y. Inoue (1994) Distinct distributions of five NMDA receptor channel subunit mRNAs in the brainstem. J. Comp. Neurol. 343:520-531.
95. Webster, W.R. (1995) Auditory system. In G. Paxinos (ed): The Rat Nervous System, 2nd ed. New York: Academic, pp. 797-831.
96. Wenthold, R.J., D. Huie, R.A. Altschuler, and K.A. Reeks (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience 22:897-912.
97. Wenthold, R.J., C. Hunter, K. Wada, and C.J. Dechesne (1990) Antibodies to a C-terminal peptide of the rat brain glutamate receptor subunit, GluR-A, recognize a subpopulation of AMPA binding sites but not kainate sites. FEBS Lett. 276:147-150.
98. Wenthold, R.J., N. Yokotani, K. Doi, and K. Wada (1992) Immunochemical characterization of the non-NMDA glutamate receptor using subunit-specific antibodies. J. Biol. Chem. 257:501-507.
99. Wenthold, R.J., C. Hunter, and R.S. Petralia (1993) Excitatory amino acid receptors in the rat cochlear nucleus. In M.A. Merchan, J.M. Juiz, D.A. Godfrey, and E. Mugnaini (eds): The Mammalian Cochlear Nuclei. Organization and Function. New York: Plenum Press, pp. 179-194.
100. Wenthold, R.J., V.A. Trumpy, W.S. Zhu, and R.S. Petralia (1994) Biochemical and assembly properties of GluR6 and KA2, two members of the kainate receptor family, determined with subunit-specific antibodies. J. Biol. Chem. 269:1332-1339.
101. Wenthold, R.J. and R.S. Petralia (1996) Non-NMDA glutamate receptors: Molecular properties. In A.J. Turner and F.A. Stephenson (eds): Amino Acid Neurotransmission. London: Portland Press Ltd. (in press).
102. Woody, C.D., X.-F. Wang, E. Gruen, and J. Landeira-Fernandez (1992) Unit activity to click CS changes in dorsal cochlear nucleus after conditioning. Neuroreport 3:385-388.
103. Wouterlood, F.G. and E. Mugnaini (1984) Cartwheel neurons of the dorsal cochlear nucleus: A Golgi-electron microscopic study in rat J. Comp. Neurol. 227:136-157.
104. Wouterlood, F.G., E. Mugnaini, K.K. Osen, and A.-L. Dahl (1984) Stellate neurons in rat dorsal cochlear nucleus studied with combined Golgi impregnation and electron microscopy: synaptic connections and mutual coupling by gap junctions. J. Neurocytol. 13:639-664.
105. Wright, D.D., C.D. Blackstone, R.L. Huganir, and D.K. Ryugo (1993) Immunocytochemical localization of a metabotropic glutamate receptor (mGR1α) within the dorsal cochlear nucleus of the rat. Assoc. Res. Otolaryngol. Abs. 16:122.
106. Wright, D.D., C.D. Blackstone, R.L. Huganir, and D.K. Ryugo (1996) Immunocytochemical localization of the mGluR1α metabotropic glutamate receptor in the dorsal cochlear nucleus. J. Comp. Neurol. 364:729-745.
107. Wright, D.D. and D.K. Ryugo (1994) Projections from dorsal column nuclei neurons form mossy fiber-like terminals in the dorsal cochlear nucleus of rat. Assoc. Res. Otolaryngol. Abs. 17:28.
108. Wright, D.D. and D.K. Ryugo (1995) Localization of the mGluR1α metabotropic glutamate receptor in unipolar brush cells of the dorsal cochlear nucleus and cerebellum. Assoc. Res. Otolaryngol. Abs. 18:195.
109. Wright, D.D. and D.K. Ryugo (1996) Mossy fiber projections from the cuneate nucleus to the cochlear nucleus in the rat. J. Comp. Neurol. 365:159-172.
110. Young, E.D., G.A. Spirou, J.J. Rice, and H.F. Voigt (1992) Neural organization and responses to complex stimuli in the dorsal cochlear nucleus. Phil. Trans. R. Soc. Lond. B 336:407-413.
111. Young, E.D., I. Nelken, and R.A. Conley (1993) Cochlear nucleus responses evoked from the dorsal column (somatosensory) nuclei. Assoc. Res. Otolaryngol. Abs. 16:124.
112. Young, E.D., G.A. Spirou, I. Nelken, and R.A. Conley (1994) The physiology and organization of the DCN. Assoc. Res. Otolaryngol. Abs. 17:156.
113. Young, E.D., I. Nelken, and R.A. Conley (1995) Somatosensory effects on neurons in dorsal cochlear nucleus. J. Neurophysiol. 73:743-765.
114. Zhang, S. and D. Oertel (1993a) Tuberculoventral cells of the dorsal cochlear nucleus of mice: Intracellular recordings in slices. J. Neurophysiol. 69:1409-1421.
115. Zhang, S. and D. Oertel (1993b) Giant cells of the dorsal cochlear nucleus of mice: Intracellular recordings in slices. J. Neurophysiol. 69:1398-1408.
116. Zhang, S. and D. Oertel (1993c) Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: Intracellular recordings in slices. J. Neurophysiol. 69:1384-1397.
117. Zhang, S. and D. Oertel (1994) Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. J. Neurophysiol. 71:914-930.