Glycine receptors in adult guinea pig brain stem auditory nuclei: Regulation after unilateral cochlear ablation

Experimental Neurology

Volumn 154, Issue 2, 1998, Pages 473-488

  Suneja, S K ^a   Benson, C G ^a,b   Potashner, S J ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Cochlear nucleus; Deafness; Inferior Colliculus; Nuclei of the lateral lemniscus; Plasticity; Superior olive; Synaptic strength; 3H strychnine binding

Indexed keywords

GLYCINE RECEPTOR; STRYCHNINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COCHLEA; CONTROLLED STUDY; FEMALE; GUINEA PIG; HEARING IMPAIRMENT; INFERIOR COLLICULUS; MALE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DENSITY; SUPERIOR OLIVARY NUCLEUS;

EID: 0032441157     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1006/exnr.1998.6946     Document Type: Article

References (135)

1. Adams J. C., Mugnaini E. Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear. Res. 49:1990;281-298.
2. Altschuler R. A., Betz H., Parakkal M. H., Reeks K. A., Wenthold R. J. Identification of glycinergic synapses in the cochlear nucleus through immunocytochemical localization of the postsynaptic receptor. Brain Res. 369:1986;316-320.
3. Araki T., Yamano M., Murakami T., Wanaka A., Betz H., Tohyama M. Localization of glycine receptors in the rat central nervous system: An immunocytochemical analysis using monoclonal antibody. Neuroscience. 25:1988;613-624.
4. Axelsson A., Barrenas M. L. Tinnitus in noise-induced hearing loss. Noise-Induced Hearing Loss. 1992;Mosby Year Book, Boston. p. 269-276.
5. A. Intl. Rev. Neurobiol. 39:1996;53-76.
6. 3. J. Comp. Neurol. 296:1990;415-426.
7. Benson C. G., Gross J. S., Suneja S. K., Potashner S. J. Synaptophysin immunoreactivity in the cochlear nucleus after unilateral cochlear or ossicular removal. Synapse. 25:1997;243-257.
8. Benson C. G., Suneja S. K., Potashner S. J. Long-term regulation of glycine receptors in adult guinea pig cochlear nucleus and superior olivary complex after unilateral cochlear ablation. Soc. Neurosci. Abs. 21:1995;403.
9. Betz H., Kuhse J., Fischer M., Schmieden V., Laube B., Kuryatov A., Langosch D., Meyer G., Bormann J., Rundstrom N., Matzembach B., Kirsch J., Ramming M. Structure, diversity and synaptic localization of inhibitory glycine receptors. J. Physiol. 88:1994;243-248.
10. Bilak M., Kim J., Potashner S. J., Bohne B. A., Morest D. K. New growth of axons in the cochlear nucleus of adult chinchillas after acoustic trauma. Exp. Neurol. 147:1997;256-268.
11. Bledsoe S. C. Jr., Snead C. R., Helfert R. H., Prasad V., Wenthold R. J., Altschuler R. A. Immunocytochemical and lesion studies support the hypothesis that the projection from the medial nucleus of the trapezoid body to the lateral superior olive is glycinergic. Brain Res. 517:1990;189-194.
12. Bledsoe S. C. Jr., Nagase S., Miller J. M., Altschuler R. A. Deafness-induced plasticity in the mature central auditory system. NeuroReport. 7:1995;225-229.
13. Boettcher F. A., Salvi R. J. Functional changes in the ventral cochlear nucleus following acute acoustic overstimulation. J. Acoust. Soc. Am. 94:1993;2123-2134.
14. Brawer J. R., Morest D. K., Kane E. C. The neuronal architecture of the cochlear nucleus of the cat. J. Comp. Neurol. 155:1974;251-300.
15. Cant N. B. Projections to the lateral and medial superior olivary nuclei from the spherical and globular bushy cells of the anteroventral cochlear nucleus. Altschuler R. A., Bobbin R. P., Clopton B. M., Hoffmann D. W. Neurobiology of Hearing: The Central Auditory System. 1991;99-119 Raven Press, New York.
16. Caspary D. M., Faingold C. L. Non-ND. Brain Res. 503:1989;83-90.
17. Caspary D. M., Finlayson P. G. Superior olivary complex: Functional neuropharmacology of principal cell types. Altschuler R. A., Bobbin R. P., Clopton B. M., Hoffmann D. W. Neurobiology of Hearing: The Central Auditory System. 1991;141-161 Raven Press, New York.
18. Caspary D. M., Havey D. C., Faingold C. L. Effects of microiontophoretically applied glycine and GABA on neuronal response patterns in the cochlear nuclei. Brain Res. 172:1979;179-185.
19. Caspary D. M., Pazara K. E., Kossl M., Faingold C. L. Strychnine alters the fusiform cell output from the dorsal cochlear nucleus. Brain Res. 417:1987;273-282.
20. Caspary D. M., Backoff P. M., Finlayson P. G., Palombi P. S. Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. J. Neurophysiol. 72:1994;2124-2133.
21. 3. Ottersen O. P., Storm-Mathisen J. Glycine Neurotransmission. 1990;239-263 Wiley, New York.
22. Dupont J., Bonneau J. M., Altschuler R. A. GABA and glycine changes in the guinea pig brainstem auditory nuclei after total destruction of the inner ear. Assoc. Res. Otolaryngol. Abstr. 17:1994;11.
23. Evans E. F., Zhao W. Varieties of inhibition in the processing and control of processing in the mammalian cochlear nucleus. Prog. Brain Res. 97:1993;117-126.
24. Faingold C. L., Gehlbach G., Caspary D. M. Functional pharmacology of inferior colliculus neurons. Altschuler R. A., Bobbin R. P., Clopton B. M., Hoffman D. W. Neurobiology of Hearing: The Central Auditory System. 1991;223-251 Raven, New York.
25. Friauf E., Hammerschmidt B., Kirsch J. Development of adult-type inhibitory glycine receptors in the central auditory system of rats. J. Comp. Neurol. 385:1997;117-134.
26. 3. Brain Res. Bull. 15:1985;473-486.
27. Frostholm A., Rotter A. Autoradiographic localization of receptors in the cochlear nucleus of the mouse. Brain Res. Bull. 16:1986;189-203.
28. ABEptesicus fuscus. J. Comp. Neurol. 369:1996;83-92.
29. Garcia M. M., Harlan R. E. Protein kinase C in central auditory pathways of the rat. J. Comp. Neurol. 385:1997;1-25.
30. Gentschev T., Sotelo C. Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultrastructural study. Brain Res. 62:1973;37-60.
31. Gerken G. M. Central denervation hypersensitivity in the auditory system of the cat. J. Acoust. Soc. Am. 66:1979;721-727.
32. Ghosh A., Greenberg M. E. Calcium signaling in neurons: Molecular mechanisms and cellular consequences. Science. 268:1995;239-247.
33. Glendenning K. K., Baker B. N. Neuroanatomical distribution of receptors for three potential inhibitory neurotransmitters in the brainstem auditory nuclei of the cat. J. Comp. Neurol. 275:1988;288-308.
34. Glendenning K. K., Baker B. N., Hutson K. A., Masterton R. B. Acoustic chiasm V: Inhibition and excitation in the ipsilateral and contralateral projections of LSO. J. Comp. Neurol. 319:1992;100-122.
35. Godfrey D. A., Parli J. A., Dunn J. D., Ross C. D. Neurotransmitter microchemistry of the cochlear nucleus and superior olivary complex. Syka J., Masterton R. B. Auditory Pathway. 1988;107-121 Plenum Press, New York.
36. Godfrey D. A., Carter J., Lowry O. H., Matschinsky F. M. Distribution of gamma-amino-butyric acid, glycine, glutamate and aspartate in the cochlear nucleus of the rat. J. Histochem. Cytochem. 26:1978;118-126.
37. Godfrey D. A., Carter J., Berger S. J., Lowry O. H., Matschinsky F. M. Quantitative histochemical mapping of candidate transmitter amino acids in cat cochlear nucleus. J. Histochem. Cytochem. 25:1977;417-431.
38. Grothe B., Sanes D. H. Bilateral inhibition by glycinergic afferents in the medial superior olive. J. Neurophysiol. 69:1993;1192-1196.
39. Grothe B., Sanes D. H. Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons: Anin vitro. J. Neurosci. 14:1994;1701-1709.
40. Hall J. G. The cochlear nucleus in monkeys after dehydro-streptomycin or noise exposure. Acta Oto. Laryngol. 81:1976;344-352.
41. Helfert R. H., Bonneau J. M., Wenthold R. J., Altschuler R. A. GABA and glycine immunoreactivity in the guinea pig superior olivary complex. Brain Res. 501:1989;269-286.
42. Helfert R. H., Juiz J. M., Bledsoe S. C. Jr., Bonneau J. M., Wenthold R. J., Altschuler R. A. Patterns of glutamate, glycine, and GABA immunolabeling in four synaptic terminal classes in the lateral superior olive of the guinea pig. J. Comp. Neurol. 323:1992;305-325.
43. Hillyer E. V., Queensberry K. E., Donnelly T. M. Biology, husbandry and clinical techniques. Hillyer E. V., Queensberry K. E. Ferrets, Rabbits and Rodents: Clinical Medicine and Surgery. 1997;243-259 Saunders, Philadelphia.
44. Huffman R. F., Covey E. Origin of ascending projections to the nuclei of the lateral lemniscus in the big brown bat,Eptesicus fuscus. J. Comp. Neurol. 357:1995;532-545.
45. Irvine D. R. F. The auditory brainstem. Autrum A., Ottoson D., Perl E. R., Schmidt R. F., Shimazu H., Willis W. D. Progress in Sensory Neurophysiology 7. 1986;1-279 Springer-Verlag, New York.
46. Jastreboff P. J. Phantom auditory perception (tinnitus): Mechanisms of generation and perception. Neurosci. Res. 8:1990;221-254.
47. Jean-Baptiste M., Morest D. K. Transneuronal changes of synaptic endings and nuclear chromatin in the trapezoid body following cochlear ablation in cats. J. Comp. Neurol. 162:1975;111-133.
48. Kaltenbach J. A., McCaslin D. L. Increases in spontaneous activity in the dorsal cochlear nucleus following exposure to high intensity sound: A possible neural correlate of tinnitus. Auditory Neurosci. 3:1996;57-78.
49. 2+. J. Neurophysiol. 76:1996;646-650.
50. Kim J., Morest D. K., Bohne B. A. Degeneration of axons in the brain stem of the chinchilla after auditory overstimulation. Hear. Res. 103:1997;169-191.
51. Kolston J., Osen K. K., Hackney C. M., Ottersen O. P., Storm-Mathisen J. An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat. Embryol. 186:1992;443-465.
52. Kuhse J., Schmieden V., Betz H. A single amino acid exchange alters the pharmacology of neonatal rat glycine receptor subunit. Neuron. 5:1990;867-873.
53. Kurino M., Fukunaga K., Ushio Y., Miyamoto E. Activation of mitogen-activated protein kinase in cultured rat hippocampal neurons by stimulation of glutamate receptors. J. Neurochem. 65:1995;1282-1289.
54. Kuwabara N., Zook J. M. Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. J. Comp. Neurol. 324:1992;522-538.
55. Kuwabara N., DiCaprio R. A., Zook J. M. Afferents to the medial nucleus of the trapezoid body and their collateral projections. J. Comp. Neurol. 314:1991;684-706.
56. Lachica E. A., Zirpel L., Rubel E. W. Intracellular mechanisms involved in the afferent regulation in the avian cochlear nucleus. Salvi R. J., Henderson D., Fiorini F., Colletti V. Auditory System Plasticity and Regeneration. 1996;333-353 Thieme Medical Publishers, New York.
57. Lachica E. A., Rubsamen R., Zirpel L., Rubel E. W. Glutamatergic inhibition of voltage-operated calcium channels in the avian cochlear nucleus. J. Neurosci. 15:1995;1724-1734.
58. LeBeau F. E., Rees A., Malmierca M. S. Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. J. Neurophysiol. 75:1996;902-919.
59. +. Neuroscience. 3:1978;1069-1074.
60. Malosio L., Pouey B. M., Kuhse J., Betz H. Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J. 10:1991;2401-2409.
61. McCormick J. G., Nuttall A. L. Auditory research. Wagner J. E., Manning P. J. The Biology of the Guinea Pig. 1976;282-303 Academic Press, New York.
62. The Microcomputer Imaging Device, M2 and M4, Operations Manual. 1995;Imaging Research Inc. Saint Catharines. p. 13-33.
63. 3. Neuroscience. 67:1995;713-719.
64. Molitor S., Manis P. B. Evidence for functional metabotropic glutamate receptors in the dorsal cochlear nucleus. J. Neurophysiol. 77:1997;1889-1905.
65. Moore D. R. Auditory brainstem of the ferret: Early cessation of developmental sensitivity of neurons in the cochlear nucleus to removal of the cochlea. J. Comp. Neurol. 302:1990;810-823.
66. Moore D. R. Auditory brainstem of the ferret: Long survival following cochlear removal progressively changes projections from the cochlear nucleus to the inferior colliculus. J. Comp. Neurol. 339:1994;301-310.
67. Moore D. R., Kowalchuk N. E. Auditory brainstem of the ferret: Effects of unilateral cochlear lesions on cochlear nucleus volume and projections to the inferior colliculus. J. Comp. Neurol. 272:1988;503-515.
68. Morest D. K., Bohne B. Noise-induced degeneration in the brain and representation of inner and outer hair cells. Hear. Res. 9:1983;145-151.
69. Morest D. K., Oliver D. L. The neuronal architecture of the inferior colliculus in the cat: Defining the functional anatomy of the auditory midbrain. J. Comp. Neurol. 222:1984;209-236.
70. Morest D. K., Kim J., Bohne B. A. Neuronal and transneuronal degeneration of auditory axons in the brainstem after cochlear lesions in the chinchilla: Cochleotopic and non-cochleotopic patterns. Hear. Res. 103:1997;151-168.
71. Musgrave M. A., Madigan M. A., Bennett B. A., Goh J. W. Stimulation of postsynaptic and inhibition of presynaptic adenylyl cyclase activity by metabotropic glutamate activation. J. Neurochem. 62:1994;2316-2324.
72. Nakanishi S. Metabotropic glutamate receptors: Synaptic transmission, modulation, and plasticity. Neuron. 13:1994;1031-1037.
73. Nishizaki T., Ikeuchi Y. Activation of endogenous protein kinase C enhances currents through α1 and α2 glycine receptor channels. Brain Res. 687:1995;214-216.
74. Oertel D., Wickesberg R. E. Glycinergic inhibition in the cochlear nuclei: Evidence for tuberculoventral neurons being glycinergic. Merchan M. A., Jiuz J. M., Godfrey D. A., Mugnaini E. The Mammalian Cochlear Nuclei: Organization and Function. 1993;225-237 Plenum Press, New York.
75. Ohishi H., Akazawa C., Shigemoto R., Nakanishi S., Mizuno N. Distributions of the mRNAs forL. J. Comp. Neurol. 360:1995;555-570.
76. Ohishi H., Shigemoto R., Nakanishi S., Mizuno N. Distributions of the mRNAs for a metabotropic glutamate receptor (mGluR3) in the rat brain: Anin situ. J. Comp. Neurol. 335:1993;252-266.
77. Oliver D. L., Huerta M. F. Inferior and superior colliculi. Webster D. B., Popper A. N., Fay R. R. The Mammalian Auditory Pathway: Neuroanatomy. 1992;168-221 Springer-Verlag, New York.
78. Ostapoff E.-M., Benson C. G., Saint Marie R. L. GABA- and glycine-immunoreactive projections from the superior olivary complex to the cochlear nucleus in guinea pigs. J. Comp. Neurol. 381:1997;500-512.
79. Palacios J. M., Cortes R., Dietl M. M. A laboratory guide for the in vitro labeling of receptors in tissue sections for autoradiography. van Leeuwen F. W., Buijs R. M., Pool C. W., Pach O. Molecular Neuroanatomy: Techniques in the Behavioral and Neural Sciences. 1988;95-109 Elsevier, Amsterdam.
80. Petralia R. S., Wenthold R. J. Light and electron immunocytochemical localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318:1992;329-354.
81. Petralia R. S., Wang Y., Zhao H., Wenthold R. J. Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. J. Comp. Neurol. 372:1996;356-383.
82. Pin J-P., Duvoisin R. The metabotropic glutamate receptors: Structure and function. Neuropharmacology. 34:1995;1-26.
83. Potashner S. J. Uptake and release ofD. J. Neurochem. 41:1983;1094-1101.
84. Potashner S. J., Benson C. G., Ostapoff E.-M., Lindberg N., Morest D. K. Glycine and GABA: Transmitter candidates of projections descending to the cochlear nucleus. Merchan M. A., Jiuz J. M., Godfrey D. A., Mugnaini E. The Mammalian Cochlear Nuclei: Organization and Function. 1993;195-210 Plenum Press, New York.
85. Potashner S. J., Suneja S. K., Benson C. G. Regulation of D-aspartate release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exptl. Neurol. 148:1997;222-235.
86. Powell T. P. S., Erulkar S. D. Transneuronal cell degeneration in the auditory relay nuclei of the cat. J. Anat. 96:1962;249-268.
87. 3. Neuroscience. 17:1986;11-35.
88. Rajan R., Irvine D. R. F., Wise L. Z., Heil P. Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex. J. Comp. Neurol. 338:1993;17-49.
89. Robertson D., Irvine D. R. F. Plasticity of frequency organization in auditory cortex of guinea pigs with unilateral deafness. J. Comp. Neurol. 282:1989;456-471.
90. Rubio M. E., Wenthold R. J. Glutamate receptors are selectively targeted to postsynaptic sites in neurons. Neuron. 18:1997;939-950.
91. 3. Brain Res. 524:1990;244-253.
92. Saint Marie R. L., Benson C. G., Ostapoff E-M., Morest D. K. Glycine immunoreactive projection from the dorsal to the anteroventral cochlear nucleus. Hear. Res. 51:1991;11-28.
93. Saint Marie R. L., Ostapoff E-M., Morest D. K., Wenthold R. J. A glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance. J. Comp. Neurol. 279:1989;382-396.
94. Salvi R. J., Powers N. L., Saunders S. S., Boettcher F. A., Clock A. Enhancement of evoked response amplitude and single unit activity after noise exposure. Dancer A. L., Henderson D., Salvi R. J., Hamernik R. P. Noise-Induced Hearing Loss. 1992;156-171 Mosby, St. Louis.
95. Sanes D. H., Wooten G. F. Development of glycine receptor distribution in the lateral superior olive of the gerbil. J. Neurosci. 7:1987;3803-3811.
96. Sanes D. H., Geary W. A., Wooten J. F., Rubel E. W. Quantitative distribution of the glycine receptor in the auditory brain stem of the gerbil. J. Neurosci. 7:1987;3793-3802.
97. Sato K., Kuriyama H., Altschuler R. A. Expression of glycine receptor subunits in the cochlear nucleus and superior olivary complex using non-radioactive in situ hybridization. Hear. Res. 91:1995;7-18.
98. Saunders J. C., Dear S. P., Schneider M. E. The anatomical consequences of acoustic injury: A review and tutorial. J. Acoust. Soc. Am. 78:1985;833-860.
99. Saunders J. C., Cohen Y. E., Szymko Y. M. The structural and functional consequences of acoustic injury in the cochlear and peripheral auditory system: A five year update. J. Acoust. Soc. Am. 90:1991;136-146.
100. Schwartz I. R. The superior olivary complex and lateral lemniscal nuclei. Webster D. B., Popper A. N., Fay R. R. The Mammalian Auditory Pathway: Neuroanatomy. 1992;117-167 Springer-Verlag, New York.
101. Sie K. C., Rubel E. W. Rapid changes in protein synthesis and cell size in the cochlear nucleus following eighth nerve activity blockade or cochlea ablation. J. Comp. Neurol. 320:1992;501-508.
102. Smith P. H., Joris P. X., Yin T. C. T. Projections of physiologically characterized spherical bushy cells from the cochlear nucleus of the cat: Evidence for delay lines to the medial superior olive. J. Comp. Neurol. 331:1993;245-260.
103. Spangler K. M., Cant N. B., Henkel C. K., Farley G. R., Warr W. B. Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J. Comp. Neurol. 259:1987;452-465.
104. Spangler K. M., Warr W. B., Henkel C. K. The projections of principal cells of the medial nucleus of the trapezoid body in the cat. J. Comp. Neurol. 238:1985;249-262.
105. Staatz-Benson C., Potashner S. J. Uptake and release of glycine in the guinea pig cochlear nucleus. J. Neurochem. 49:1987;128-137.
106. Staatz-Benson C., Potashner S. J. Uptake and release of glycine in the guinea pig cochlear nucleus after axotomy of afferent or centrifugal fibers. J. Neurochem. 51:1988;370-379.
107. Suneja S. K., Benson C. G., Potashner S. J. Modulation of strychnine binding in the lateral lemniscal nuclei after cochlear ablation. Soc. Neurosci. Abs. 21:1995;404.
108. 3. Assoc. Res. Otolaryngol. Abs. 20:1997;84.
109. Suneja S. K., Benson C. G., Gross J., Potashner S. J. Evidence for glutamatergic projections from the cochlear nucleus to the superior olive and the ventral nucleus of the lateral lemniscus. J. Neurochem. 64:1995;161-171.
110. Suneja S. K., Benson C. G., Gross J., Potashner S. J. Uptake and release of D-aspartate, GABA and glycine in guinea pig brain stem auditory nuclei. J. Neurochem. 64:1995;147-160.
111. Suneja S. K., Potashner S. J., Benson C. G. Regulation of AMPA binding in the lateral lemniscus and the inferior colliculus after cochlear ablation. Soc. Neurosci. Abst. 23:1997;184.
112. Suneja S. K., Potashner S. J., Benson C. G. Plastic changes in glycine and GABA release and uptake in adult brain stem auditory nuclei after unilateral middle ear ossicle removal and cochlear ablation. Exp. Neurol. 151:1998;273-288.
113. Theopold H. M. Degenerative alterations in the central cochlear nucleus of the guinea pig after impulse noise exposure. A preliminary light and electron microscopic study. Arch. Oto. Rhino. Laryngol. 209:1975;247-262.
114. Vaello M-L., Ruiz-Gomez A., Lerma J., Mayor F. Jr. Modulation of inhibitory glycine receptors by phosphorylation by protein kinase C and cAMP-dependent protein kinase. J. Biol. Chem. 269:1994;2002-2008.
115. Vater M., Covey E., Casseday J. H. The columnar region of the ventral nucleus of the lateral lemniscus in the big brown bat (Eptesicus fuscus. Cell Tissue Res. 289:1997;223-233.
116. Wang Y. X., Wenthold R. J., Ottersen O. P., Petralia R. S. Endbulb synapses in the anteroventral cochlear nucleus express a specific subset of AMPA-type glutamate receptor subunits. J. Neurosci. 18:1998;1148-1160.
117. Warr W. B. Organization of olivocochlear efferent systems in mammals. Webster D. B., Popper A. N., Fay R. R. The Mammalian Auditory Pathway: Neuroanatomy. 1992;410-448 Springer-Verlag, New York.
118. Warr W. B., Beck J. E. Multiple projections from the ventral nucleus of the trapezoid body in the rat. Hear. Res. 93:1996;83-101.
119. Webster D. B., Webster M. Long-term effects of cochlear nerve destruction on the cochlear nuclei. Anat. Rec. 190:1978;578.
120. Wenthold R. J. Evidence for a glycinergic pathway connecting the two cochlear nuclei: An immunocytochemical and retrograde transport study. Brain Res. 415:1987;183-187.
121. Wenthold R. J., Gulley R. L. Aspartic acid and glutamic acid levels in the cochlear nucleus after auditory nerve lesion. Brain Res. 138:1977;111-123.
122. Wenthold R. J., Huie D., Altschuler R. A., Reeks K. A. Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience. 22:1987;897-912.
123. Wenthold R. J., Parakkal M. H., Oberdorfer M. D., Altschuler R. A. Glycine receptor immunoreactivity in the ventral cochlear nucleus of the guinea pig. J. Comp. Neurol. 276:1988;423-435.
124. Wickesberg R. E., Oertel D. Delayed, frequency-specific inhibition in the cochlear nuclei of mice: A mechanism for monaural echo suppression. J. Neurosci. 10:1990;1762-1768.
125. Wickesberg R. E., Whitlon D., Oertel D. Tuberculoventral neurons project to the multipolar cell area but not to the Octopus cell area of the posteroventral cochlear nucleus. J. Comp. Neurol. 313:1991;457-468.
126. Wickesberg R. E., Whitlon D., Oertel D. In vitro modulation of somatic glycine-like immunoreactivity in presumed glycinergic neurons. J. Comp. Neurol. 339:1994;311-327.
127. Willott J. F., Lu S. M. Noise-induced hearing loss can alter neural coding and increase excitability in the central nervous system. Science. 216:1982;1331-1332.
128. Wright D. D., Blackstone C. D., Huganir R. L., Ryugo D. K. Immunocytochemical localization of the mGluR1-alpha metabotropic glutamate receptor in the dorsal cochlear nucleus. J. Comp. Neurol. 364:1996;729-745.
129. Wu S. H., Oertel D. Inhibitory circuitry in the ventral cochlear nucleus is probably mediated by glycine. J. Neurosci. 6:1986;2691-2706.
130. Wu S. H., Kelly J. B. Synaptic pharmacology of the superior olivary complex studied in mouse brain slice. J. Neurosci. 12:1992;3084-3097.
131. Wu S. H., Kelly J. B. Physiological evidence for ipsilateral inhibition in the lateral superior olive: Synaptic responses in mouse brain slice. Hear. Res. 73:1994;57-64.
132. Wu S. H., Kelly J. B. Inhibition in the superior olivary complex: pharmacological evidence from mouse brain slice. J. Neurophysiol. 73:1995;256-269.
133. Wu S. H., Kelly J. B. In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. III. Synaptic pharmacology. J. Neurophysiol. 75:1996;1271-1282.
134. Zirpel L., Lachica E. A., Rubel E. W. Activation of a metabotropic glutamate receptor increases intracellular calcium concentrations in neurons of the avian cochlear nucleus. J. Neurosci. 15:1995;214-222.
135. Zirpel L., Nathanson N. M., Rubel E. W., Hyson R. L. Glutamate-stimulated phosphatidylinositol metabolism in the avian cochlear nucleus. Neurosci Lett. 168:1994;163-166.