N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus

Journal of Neurophysiology

Volumn 76, Issue 3, 1996, Pages 1639-1656

  Manis, Paul B ^a   Molitor, Scott C ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; 6,7 DINITRO 2,3 QUINOXALINEDIONE; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; COCHLEAR NUCLEUS; CONTROLLED STUDY; DOSE RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GUINEA PIG; INTRACELLULAR RECORDING; LATENT PERIOD; NERVE FIBER; NERVE STIMULATION; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC POTENTIAL; TISSUE DISTRIBUTION; VOLTAGE CLAMP;

EID: 0029744957     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.3.1639     Document Type: Article

References (96)

1. AKAIKE, N., KANEDA, M., HORI, N., AND KRISHTAL, O. A. Blockade of the N-methyl-D-aspartate response in enzyme-treated rat hippocampal neurons. Neurosci. Lett. 87: 75-79, 1988.
2. ALLEN, C. N., BRADY, R., SWANN, J., HORI, N., AND CARPENTER, D. O. N-methyl-D-aspartate receptors are inactivated by trypsin. Brain Res. 458: 147-150, 1988.
3. AUDINAT, E., KNOPFEL, T., AND GAHWILER, B. H. Responses to excitatory amino acids of Purkinje cells and neurones of the deep nuclei in cerebellar slice cultures. J. Physiol. Lond. 430: 297-313, 1990.
4. BALOGH, A. E. Muscarinic Modulation of Parallel Fiber Synaptic Transmission in the Dorsal Cochlear Nucleus (PhD dissertation). Baltimore, MD: Johns Hopkins University, 1995.
5. BEKKERS, J. M. AND STEVENS, C. F. NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature Lond. 341: 230-233, 1989.
6. BERREBI, A. S., MORGAN, J. I., AND MUGNAINI, E. The Purkinje cell class may extend beyond the cerebellum. J. Neurocytol. 19: 643-654, 1990.
7. BERREBI, A. S. AND MUGNAINI, E. Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anal. Embryol. 183: 427-454, 1991.
8. BILAK, S., BILAK, M., AND MOREST, D. K. N-methyl-D-aspartate receptor (NMDAR) expression in mouse cochlear nucleus (CN) neuronal cell types compared to cerebellar cortex. Abstr. Assoc. Res. Otolaryngol. 18: 31, 1995.
9. BIRD, S. J., GULLEY, R. L., WENTHOLD, R. J., AND FEX, J. Kainic acid injections result in degeneration of cochlear nucleus cells innervated by the auditory nerve. Science Wash. DC 202: 1087-1089, 1978.
10. BLACKSTAD, T. W., OSEN, K. K., AND MUGNAINI, E. Pyramidal neurones of the dorsal cochlear nucleus: a Golgi and computer reconstruction study in cat. Neuroscience 13: 827-854, 1984.
11. BOOTH, R. F. G., PATEL, T. B., AND CLARK, J. B. The development of enzymes of energy metabolism in the brain of a precocial (guinea pig) and nonprecocial (rat) species. J. Neurochem. 34: 17-25, 1980.
12. BRAWER, J. R., MOREST, D. K., AND KANE, E. C. The neuronal architecture of the cochlear nucleus of the cat. J. Comp. Neurol. 155: 251-300, 1974.
13. CLEMENTS, J. D., LESTER, R. A., TONG, G., JAHR, C. E., AND WESTBROOK, G. L. The time course of glutamate in the synaptic cleft. Science Wash. DC 258: 1498-1501, 1992.
14. COLLINGRIDGE, G. L. AND LESTER, R. A. J. Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 41: 143-210, 1989.
15. CONNORS, B. W. AND PRINCE, D. A. Effects of local anesthetic QX-314 on the membrane properties of hippocampal pyramidal neurons. J. Pharmacol. Exp. Ther. 220: 476-481, 1982.
16. CREPEL, F. AND AUDINAT, E. Excitatory amino acid receptors of cerebellar Purkinje cells: development and plasticity. Prog. Biophys. Mol. Biol. 55: 31-46, 1991.
17. DE SCHUTTER, E. Cerebellar long-term depression might normalize excitation of Purkinje cells: a hypothesis. Trends Neurosci. 18:291-295, 1995.
18. DUPONT, J. L., GARDETTE, R., AND CREPEL, F. Postnatal development of the chemosensitivity of rat cerebellar Purkinje cells to excitatory amino acids. An in vitro study. Brain Res. 431: 59-68, 1987.
19. ECCLES, J. C., LLINÁS, R. R., AND SASAKI, K. Parallel fibre stimulation and the responses induced thereby in the Purkinje cells of the cerebellum. Exp. Brain Res. 1: 17-39, 1966.
20. EDWARDS, F. A., KONNERTH, A., SAKMANN, B., AND TAKAHASHI, T. A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pfluegers Arch. 414: 600-612, 1989.
21. EILERS, J., AUGUSTINE, G. J., AND KONNERTH, A. Subthreshold synaptic Ca2+ signalling in fine dendrites and spines of cerebellar Purkinje neurons. Nature Lond. 373: 155-158, 1995.
22. FREEMAN, J. A. AND NICHOLSON, C. Experimental optimization of current source-density technique for Anuran cerebellum. J. Neurophysiol. 38: 369-382, 1975.
23. GARTHWAITE, G., YAMINI, B., AND GARTHWAITE, J. Selective loss of Purkinje and granule cell responsiveness to N-methyl-D-aspartate in rat cerebellum during development, Dev. Brain Res. 36: 288-292, 1987.
24. GRACE, A. A. AND LLINÁS, R. R. Morphological artifacts induced in intracellularly stained neurons by dehydration: circumvention using rapid dimethyl sulfoxide clearing. Neuroscience 16: 461-475, 1985.
25. 3H] glutamate-binding sites in rat central nervous system. J. Neurosci. 4: 2133-2144, 1984.
26. HACKETT, J. T., Hou, S. M., AND COCHRAN, S. L. Glutamate and synaptic depolarization of Purkinje cells evoked by parallel fibers and by climbing fibers. Brain Res. 170: 377-380, 1979.
27. HACKNEY, C. M., OSEN, K. K., AND KOLSTON, J. Anatomy of the cochlear nuclear complex of guinea pig. Anal. Embryol. 182: 123-149, 1990.
28. HESTRIN, S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature Lond. 357: 686-689, 1992.
29. HESTRIN, S., NICOLL, R. A., PERKEL, D. J., AND SAH, P. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J. Physiol. Lond. 422: 203-225, 1990.
30. HIRSCH, J. A. AND OERTEL, D. Intrinsic properties of neurones in the dorsal cochlear nucleus of mice, in vitro. J. Physiol. Lond. 396: 535-548, 1988.
31. HONORÉ, T., DAVIES, S. N., DREJER, J., FLETCHER, E. J., JACOBSEN, P., LODGE, D., AND NIELSEN, F. E. Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. Science Wash. DC 241: 701-704, 1988.
32. HORNER, K. C., SERVIERE, J., AND DEFERRE-GRANIER, C. Deoxyglucose demonstration of in-utero hearing in the guinea pig foetus. Hear. Res. 26: 327-333, 1987.
33. ISAACSON, J. S. AND WALMSLEY, B. Receptors underlying excitatory synaptic transmission in slices of the rat anteroventral cochlear nucleus. J. Neurophysiol. 73: 964-973, 1995.
34. ITO, M., SAKURAI, M., AND TONGROACH, P. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J. Physiol. Lond. 324: 113-134, 1982.
35. JOHNSON, J. W. AND ASCHER, P. Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature Lond. 325: 529-531, 1987.
36. KACHAR, B. Asymmetric illumination contrast: a method of image formation for video light microscopy. Science Wash. DC 227: 766-768, 1985.
37. KAY, A. R. AND CONNOR, J. A. Preservation of the NMDA response of neurons acutely dissociated from the mature guinea pig hippocampus. J. Neurosci. Methods 33: 77-79, 1990.
38. KAY, A. R., MILES, R., AND WONG, R. K. S. Intracellular fluoride alters the kinetic properties of calcium currents facilitating the investigation of synaptic events in hippocampal neurons. J. Neurosci. 6: 2915-2920, 1986.
39. KAY, A. R. AND WONG, R. K. S. Isolation of neurons suitable for patch clamping from adult mammalian central nervous system. J. Neurosci. Methods 16: 227-238, 1986.
40. KOLSTON, J., OSEN, K. K., HACKNEY, C. M., OTTERSEN, O. P., AND STORMMATHISEN, J. An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat. Embryol. 186: 443-465, 1992.
41. KONNERTH, A., KELLER, B. U., BALLANYI, K., AND YAARI, Y. Voltage sensitivity of NMDA-receptor mediated postsynaptic currents. Exp. Brain Res. 81: 209-212, 1990.
42. 2+ channels can transiently potentiate excitatory synaptic transmission in the hippocampus. Neuron 9: 1175-1183, 1992.
43. LESTER, R. A. J., CLEMENTS, J. D., WESTBROOK, G. L., AND JAHR, C. E. Channel kinetics determine the time course of NMDA receptor mediated synaptic currents. Nature Lond. 346: 565-567, 1990.
44. LINDEN, D. J. Long term synaptic depression in the mammalian brain. Neuron 121: 457-472, 1994.
45. LORENTE DE NÓ, R. The Primary Acoustic Nuclei. New York: Raven, 1981.
46. MACDERMOTT, A. B., MAYER, M. L., WESTBROOK, G. L., SMITH, S. J., AND BARKER, J. L. NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurons. Nature Lond. 321: 519-522, 1986.
47. MACVICAR, B. A. Infrared video microscopy to visualize neurons in the in vitro brain slice preparation. J. Neurosci. Methods 12: 133-139, 1984.
48. MANIS, P. B. Evidence for functional NMDA-type receptors in the guinea pig dorsal cochlear nucleus. Abstr. Assoc. Res. Otolaryngol. 12: 60, 1989a.
49. MANIS, P. B. Responses to parallel fiber stimulation in the guinea pig dorsal cochlear nucleus in vitro. J. NeurophysioL 61: 149-161, 1989b.
50. MANIS, P. B. Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J. Neurosci. 10: 2338-2351, 1990.
51. MANIS, P. B. AND BROWNELL, W. E. Synaptic organization of eighth nerve afferents to cat dorsal cochlear nucleus. J. Neurophysiol. 50: 1156-1181, 1983.
52. MANIS, P. B. AND MARX, S. O. Outward currents in isolated ventral cochlear nucleus neurons. J. Neurosci. 11: 2865-2880, 1991.
53. MANIS, P. B. AND MOLITOR, S. C. Identification of cells possessing NMDA receptors in the guinea pig dorsal cochlear nucleus. Soc. Neurosci. Abstr. 19: 534, 1993.
54. MANIS, P. B. AND MOLITOR, S. C. Evoked calcium transients in dendrites of rat dorsal cochlear nucleus neurons. Abstr. Assoc. Res. Otolaryngol. 19: 169, 1996.
55. MANIS, P. B., SPIROU, G. A., WRIGHT, D. D., PAYDAR, S., AND RYUGO, D. K. Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J. Comp. Neurol. 348: 261-276, 1994.
56. MAYER, M. L. AND WESTBROOK, G. L. The physiology of excitatory amino acids in the vertebrate central nervous system. Prog. Neurobiol. 28: 197-276, 1987.
57. MIYAKAWA, H., LEV -RAM, V., LASSER-ROSS, N., AND ROSS, W. N. Calcium transients evoked by climbing fiber and parallel fiber synaptic inputs in guinea pig cerebellar Purkinje neurons. J. Neurophysiol. 68: 1178-1189, 1992.
58. MOLITOR, S. C. AND MANIS, P. B. Voltage-sensitive calcium conductances in isolated guinea pig dorsal cochlear nucleus neurons. Abstr. Assoc. Res. Otolaryngol. 17: 16, 1994.
59. 3H]glutamate-binding sites in rat brain. J. Neurosci. 5: 2909-2919, 1985.
60. MONYER, H., SPRENGEL, R., SCHOEPFER, R., HERB, A., HIGUCHI, M., LOMELI, H., BURNASHEV, N., SAKMANN, B., AND SEEBURG, P. H. Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science Wash. DC 256: 1217-1221, 1992.
61. MONYER, H., BURNASHEV, N., LAURIE, D. J., SAKMANN, B., AND SEEBURG, P. H. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12: 529-540, 1994.
62. MUGNAINI, E. GABA neurons in the superficial layers of the rat dorsal cochlear nucleus: light and electron microscopic immunocytochemistry. J. Comp. Neurol. 235: 61-81, 1985.
63. MUGNAINI, E., BERREBI, A. S., DAHL, A. L., AND MORGAN, J. I. The polypeptide PEP-19 is a marker for Purkinje neurons in cerebellar cortex and cartwheel neurons in the dorsal cochlear nucleus. Arch. Ital. Biol 126: 41-67, 1987.
64. MUGNAINI, E., FLORIS, A., AND WRIGHT-GOSS, M. Extraordinary synapses of the unipolar brush cell: an electron microscopic study in the rat cerebellum. Synapse 16: 284-311, 1994.
65. MUGNAINI, E. AND MORGAN, J. I. The neuropeptide cerebellin is a marker for two similar neuronal circuits in rat brain. Proc. Natl Acad. Sci. USA 84: 8692-8696. 1987.
66. NICHOLSON, C. AND FREEMAN, J. A. Theory of current souce-density analysis and determination of conductivity tensor for Anuran cerebellum. J. Neurophysiol. 38: 356-368, 1975.
67. NOWAK, L., BREGESTOVSKI, P., ASCHER, P., HERBET, A., AND PROCHIANTZ, A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature Lond. 307: 462-465, 1984.
68. OERTEL, D. AND WU, S. H. Morphology and physiology of cells in slice preparations of the dorsal cochlear nucleus of mice. J. Comp. Neurol. 283: 228-247, 1989.
69. PATEL, T. B. AND CLARK, J. B. Comparison of the development of the fatty acid content and composition of the brain of a precocial species (guinea pig) and a nonprecocial species (rat). J. Neurochem. 35: 149-154, 1980.
70. PETRALIA, R. S., YOKOTANI, N., AND WENTHOLD, R. J. 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, 1994.
71. PEYERT, D., GEFFARD, M., AND ARAN, J.-M. GABA immunoreactivity in the primary nuclei of the auditory central nervous system. Hear. Res. 23: 115-121, 1986.
72. RHODE, W. S., SMITH, P. H., AND OERTEL, D. Physiological response properties of cells labeled intracellularly with horseradish peroxidase in cat dorsal cochlear nucleus. J. Comp. Neurol. 213: 426-447, 1983.
73. ROMAND, R. Maturation des potentiels cochlearies dans la periode perinatale chez le chat et chez le Cobaye. J. Physiol. Paris 63: 763-782, 1971.
74. RYUGO, D. K., PONGSTAPORN, T., WRIGHT, D. D., AND SHARP, A. H. Inositol 1,4,5-trisphosphate receptors: immunocytochemical localization in the dorsal cochlear nucleus. J. Comp. Neurol. 358: 102-118, 1995.
75. SAH, P., HESTRIN, S., AND NICOLL, R. A. Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science Wash. DC 246: 815-818, 1989.
76. SAKURAI, M. Synaptic modification of parallel fibre-Purkinje cell transmission in in vitro guinea-pig cerebellar slices. J. Physiol. Lond. 394: 463-480, 1987.
77. SAKURAI, M. Calcium is an intracellular mediator of the climbing fiber in induction of cerebellar long-term depression. Proc. Natl. Acad. Sci. USA 87: 3383-3385, 1990.
78. SANDOVAL, M. E. AND COTMAN, C. W. Evaluation of glutamate as a neurotransmitter of cerebellar parallel fibers. Neuroscience 3: 199-206, 1978.
79. SATO, K., KURIYAMA, H., BONNEAU, J. M., AND ALTSCHULER, R. A. Expression of NMDA-receptor mRNA in the rat cochlear nucleus and superior olivary complex. Abstr. Assoc. Res. Otolaryngol. 18: 31, 1995.
80. 3H- labeled amino acids in the dorsal cochlear nucleus of the cat. An autoradiographic study. Exp. Neurol. 73: 601-617, 1981.
81. SIMON, S. M. AND LLINÁS, R. R. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys. J. 48: 485-498, 1985.
82. SMITH, P. H. AND RHODE, W. S. Electron microscopic features of physiologically characterized, HRP-labeled fusiform cells in the cat dorsal cochlear nucleus. J. Comp. Neurol. 237: 127-143, 1985.
83. SPRUSTON, N., JAFFE, D. B., WILLIAMS, S. H., AND JOHNSTON, D. Voltage-and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 70: 781-802, 1993.
84. SPRUSTON, N., JONAS, P., AND SAKMANN, B. Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J. Physiol. Lond. 482: 325-352, 1995a.
85. SPRUSTON, N., SCHILLER, Y., STUART, G., AND SAKMANN, B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science Wash. DC 268: 297-300, 1995b.
86. STUART, G. J., DODT, H.-U., AND SAKMANN, B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pfluegers Arch. 423: 511-518, 1993.
87. STUART, G. J. AND SAKMANN, B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature Lond. 367: 69-72, 1994.
88. TRUSSELL, L. O., THIO, L. L., ZORUMSKI, C. F., AND FISCHBACH, G. D. Rapid desensitization of glutamate receptors in vertebrate central neurons. Proc. Natl. Acad. Sci. USA 85: 4562-4566, 1988.
89. TURNER, R. W., MALER, L., DEERNICK, T., LEVINSON, S. R., AND ELLISMAN, M. H. TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron. J. Neurosci. 14: 6453-6471,1994.
90. WALSH, E. J., MCGEE, J., AND FITZAKERLEY, J. L. Development of glutamate and NMDA sensitivity of neurons within the cochlear nuclear com-plex of kittens. J. Neurophysiol. 69: 201-218, 1993.
91. WATANABE, M., MISHINA, M., AND INOUE, Y. Distinct distributions of five NMDA receptor channel subunit mRNAs in the brainstem. J. Comp. Neurol. 343: 520-531, 1994a.
92. WATANABE, M., MISHINA, M., AND INOUE, Y. Distinct spatiotemporal expressions of five NMDA receptor channel subunit mRNAs in the cerebellum. J. Comp. Neurol. 343: 513-519, 1994b.
93. + current in the medial entorhinal cortex. Neuron 11: 1037-1047, 1993.
94. WOUTERLOOD, F. G. AND MUGNAINI, E. Cartwheel neurons of the dorsal cochlear nucleus: a Golgi-electron microscopic study in rat. J. Comp. Neurol. 227: 136-157, 1984.
95. ZHANG, S. AND OERTEL, D. Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices. J. Neurophysiol. 69: 1384-1397, 1993.
96. ZHANG, S. AND OERTEL, D. Neuronal circuits associated with the output of the dorsal cochlear nucleus through fusiform cells. J. Neurophysiol. 71: 914-930, 1994.