Activity-dependent regulation of [Ca2+](i) in avian cochlear nucleus neurons: Roles of protein kinases A and C and relation to cell death

Journal of Neurophysiology

Volumn 79, Issue 5, 1998, Pages 2288-2302

  Zirpel, Lance ^a,b   Lippe, William R ^a   Rubel, Edwin W ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; CYCLIC AMP DEPENDENT PROTEIN KINASE; DIOCTANOIN; FORSKOLIN; FURA 2; GLUTAMATE RECEPTOR; PHORBOL 12 ACETATE 13 MYRISTATE; PROPIDIUM IODIDE; PROTEIN KINASE C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; DATA ANALYSIS; DEAFFERENTATION; ENZYME REGULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; IMAGE ANALYSIS; MAGNOCELLULAR NUCLEUS; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0031841549     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.79.5.2288     Document Type: Article

References (128)

1. BEHL, C., WIDMANN, M., TRAPP, T., AND HOLSBOER, F. 17-beta estradiol protects neurons from oxidative stress-induced cell death in vitro. Biochem. Biophys. Res. Commun. 216: 473-482, 1995.
2. BEVENSEE, M. O., SCHWIENING, C. J., AND BORON, W. F. Use of BCECF and propidium iodide to assess membrane integrity of acutely isolated CA1 neurons from rat hippocampus. J. Neurosci. Methods 58: 61-75, 1995.
3. BLEAKMAN, D., RUSIN, K. I., CHARD, P. S., GLAUM, S. R., AND MILLER, R. J. Metabotropic glutamate receptors potentiate ionotropic glutamate responses in the rat dorsal horn. Mol. Pharmacol. 42: 192-196, 1992.
4. BOCKAERT, J., PIN, J., AND FAGNI, L. Metabotropic glutamate receptors: an original family of G protein-coupled receptors. Fundam. Clin. Pharmacol. 7: 473-485, 1993.
5. BORN, D. E., DURHAM, D., AND RUBEL, E. W Afferent influences on brainstem auditory nuclei of the chick: nucleus magnocellularis neuronal activity following cochlea removal. Brain Res. 557: 37-47, 1991.
6. BORN, D. E. AND RUBEL, E. W Afferent influences on brain stem auditory nuclei of the chicken: neuron number and size following cochlea removal. J. Comp. Neurol. 231: 435-445, 1985.
7. BRUCE, A. J., SAKHI, S., SCHREIBER, S. S., AND BAUDRY, M. Development of kainic acid and N-methyl-D-aspartic acid toxicity in organotypic hippocampal cultures. Exp. Neurol. 132: 209-219, 1995.
8. BRUNJES, P. C. Unilateral naris closure and olfactory system development. Brain Res. Rev. 19: 146-160, 1994.
9. CARAFOLI, E. Intracellular calcium homeostasis. Annu. Rev. Biochem. 56: 395-433, 1987.
10. CARR, C. E. AND BOUDREAU, R. E. Central projections of auditory nerve fibers in the barn owl. J. Comp. Neurol 314: 306-318, 1991.
11. CHENG, B., CHRISTAKOS, S., AND MATTSON, M. P. Tumor necrosis factors protect neurons against metabolic-excitotoxic insults and promote maintenance of calcium homeostasis. Neuron. 12: 139-153, 1994.
12. CHOI, D. W. Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci. Lett. 58: 293-297, 1985.
13. CHOI, D. W. Excitotoxic cell death. J. Neurobiol. 23: 1261-1276, 1992.
14. CLEMENTS, J. D. Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci. 19: 163-171, 1996.
15. COHEN, J. J. AND DUKE, R. C. Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J. Immunol. 132: 38-42, 1984.
16. COLLINS, F., SCHMIDT, M. F., GUTHRIE, P. B., AND KATER, S. B. Sustained increase in intracellular calcium promotes neuronal survival. J. Neurosci. 11: 2582-2587, 1991.
17. DENGLER, W. A., SCHULTE, J., BERGER, D. P., MERTELSMANN, R., AND FIEBIG, H. H. Development of a propidium iodide fluorescence assay for proliferation and cytotoxicity assays. Anticancer Drugs 6: 522-532, 1995.
18. DUBIN, M. W., STARK, L. A., AND ARCHER, S. M. A role for action-potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. J. Neurosci. 6: 1021-1036, 1986.
19. DUVOISIN, R. M., ZHANG, C., AND RAMONELL, K. A novel metabotropic glutamate receptor expressed in the retina and olfactory bulb. J. Neurosci. 15: 3075-3083, 1995.
20. ELKABES, S., CHERRY, J. A., SCHOUPS, A. A., AND BLACK, I. B. Regulation of protein kinase C activity by sensory deprivation in the olfactory and visual systems. J. Neurochem. 60: 1835-1842, 1993.
21. 2+ dynamics after toxic doses of glutamate in cerebellar granule cells. Proc. Natl. Acad. Sci. USA 87: 8017-8021, 1990.
22. FERRIS, C. D., HUGANIR, R. L., BREDT, D. S., CAMERON, A. M., AND SNYDER, S. H. Inositol trisphosphate receptor: phosphorylation by protein kinase C and calcium calmodulin-dependent protein kinases in reconstituted lipid vesicles. Proc. Natl. Acad. Sci. USA 88: 2232-2235, 1991.
23. FRANKLIN, J. L., JOHNSON, E. M., JR. Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends Neurosci. 15: 501-508, 1992.
24. FUKAYAMA, S., TASHJIAN, A. H., JR., AND BRINGHURST, F. R. Role of protein kinase A in the regulation of cytosolic free calcium in human osteoblast-like SaOS-2 cells. Am. J. Physiol. 264 (Cell. Physiol.33 ): C464-C470, 1993.
25. 2+ influx. J. Neurochem. 65: 1061-1068, 1995.
26. GALLI, C., MEUCCI, O., SCORZIELLO, A., WERGE, T. M., CALISSANO, P., AND SCHETTINI, G. Apoptosis in cerebellar granule cells is blocked by high KC1, forskolin, and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J. Neurosci. 15: 1172-1179, 1995.
27. GARDEN, G. A., CANADY, K. S., LURIE, D. I., BOTHWELL, M., AND RUBEL, E. W A biphasic change in ribosomal conformation during transneuronal degeneration is altered by inhibition of mitochondrial, but not cytoplasmic protein synthesis. J. Neurosci. 14: 1994-2008, 1994.
28. GHOSH, A. AND GREENBERG, M. E. Calcium signalling in neurons: molecular mechanisms and cellular consequences. Science 268: 239-247, 1995.
29. GLAUM, S. R. AND MILLER, R. J. Activation of metabotropic glutamate receptors produces reciprocal regulation of ionotropic glutamate and GABA responses in the nucleus of the tractus solitarius of the rat. J. Neurosci 13: 1636-1641, 1993.
30. GLOBUS, A. Brain morphology as a function of presynaptic morphology and activity. In: The Developmental Neuropsychology of Sensory Deprivation. New York: Academic Press, 1975, p. 9-91.
31. GRAY, D.W.R. AND MORRIS, P. J. The use of fluoroscein diacetate and ethidium bromide as a Viability stain for isolated Islets of Langerhans. Stain Technol. 62: 373-382, 1987.
32. GREENGARD, P., JEN, J., NAIRN, A. C., AND STEVENS, C. F. Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampai neurons. Science 253: 1135-1138, 1991.
33. GRIERSON, J. P. AND MELDOLESI, J. Calcium homeostasis in mouse fibroblast cells: affected by U-73122, a putative phospholipase Cβ blocker, via multiple mechanisms. Br. J. Pharmacol. 115: 11-14, 1995.
34. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260: 3440-3450, 1985.
35. HAAK, L. L., HELLER, C., AND VAN DEN POL, A. N. Metabotropic glutamate receptor activation modulates kainate and serotonin calcium response in astrocytes. J. Neurosci. 17: 1825-1837, 1997.
36. 2+-ATPase function in cardiac and slow-twitch skeletal muscle sarcoplasmic reticulum. Mol. Cell. Biochem. 142: 131-138, 1995.
37. HIDAKA, H. AND KOBAYASHI, R. Pharmacology of protein kinase inhibitors. Annu. Rev. Pharmacol. Toxicol. 32: 377-397, 1992.
38. HILLE, B. G protein-coupled mechanisms and nervous signaling. Neuron 9: 187-195, 1992.
39. HUBEL, D. H. AND WIESEL, T. N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond.) 206: 419-436, 1970.
40. HYDE, G. E. AND DURHAM, D. Increased deafferentation-induced cell death in chick brainstem auditory neurons following blockade of mitochondrial protein synthesis with chloramphenicol. J. Neurosci. 14: 291-300, 1994a.
41. HYDE, G. E. AND DURHAM, D. Rapid increase in mitochrondial volume in nucleus magnocellularis neurons following cochlea removal. J. Comp. Neurol. 339: 27-48, 1994b.
42. HYSON, R. L. AND RUBEL, E. W Transneuronal regulation of protein synthesis in the brain stem auditory system of the chick requires synaptic activation. J. Neurosci. 9: 2835-2845, 1989.
43. INCE, C., VAN DISSEL, J. T., AND DIESSELHOFF, M.M.C. A teflon culture dish for high-magnification microscopy and measurements in single cells. Pflügers Arch. 403: 240-244, 1985.
44. JACKSON, H., NEMETH, E. F., AND PARKS, T. N. Non-N-methyl-D-aspartate receptors mediating synaptic transmission in the avian cochlear nucleus: effects of kynurenic acid, dipicolinic acid and streptomycin. Neuroscience 16: 171-179, 1985.
45. JIANG, T., GRANT, R. L., AND ACOSTA, D. A digitized fluorescence imaging study of intracellular free calcium, mitochondrial integrity and cytotoxicity in rat renal cells exposed to ionomycin, a calcium ionophore. Toxicology 85: 41-65, 1993.
46. JOHNSON, M. E., GORES, G. J., UHL, C. B., AND SILL, J. C. Cytosolic free calcium and cell death during metabolic inhibition in a neuronal cell line. J. Neurosci. 14: 4040-4049, 1994.
47. JONAS, P. AND SPRUSTON, N. Mechanisms shaping glutamate-mediated excitatory postsynaptic currents in the CNS. Curr. Opin. Neurobiol. 4: 366-372, 1994.
48. KAISER, P. K. AND LIPTON, S. A. VIP-mediated increase in cAMP prevents tetrodotoxin-induced retinal ganglion cell death in vitro. Neuron 5: 373-381, 1990.
49. 2+ stores in brainstem auditory neurons. J. Neurophysiol. 76: 646-650, 1996.
50. KEBABIAN, J. W. The cyclic AMP cascade: a signal transduction system. Neurotransmissions 8: 1-4, 1992.
51. KELSO, S. R., NELSON, T. E., AND LEONARD, J. P. Protein kinase c-mediated enhancement of NMDA currents by metabotropic glutamate receptors in Xenopus oocytes. J. Physiol. (Lond.) 449: 705-718, 1992.
52. KENNEDY, M. B. Regulation of neuronal function by calcium. Trends Neurosci. 12: 417-419, 1989.
53. KIKKAWA, U., KITANO, T., SAITO, N., KISHIMOTO, A., TANIYAMA, K., TANAKA, C., AND NISHIZUKA, Y. Role of protein kinase C in calcium-mediated signal transduction. In: Calcium and the Cell. Chichester, UK: Wiley, 1986, p. 197-211.
54. KINNEY, G. A. AND SLATER, N. T. Potentiation of NMDA receptor-mediated transmission in turtle cerebellar granule cells by activation of metabotropic glutamate receptors. J. Neurophysiol. 69: 585-594, 1993.
55. 2+ determine nerve growth factor dependence of sympathetic ganglion cells. Proc. Natl. Acad. Sci. USA 86: 6421-6425, 1989.
56. KOLBER, M. A., QUINONES, R. R., GRESS, R. E., HENKART, P. A. Measurement of cytotoxicity by target cell release and retention of the fluorescent dye bis-carboxyethyl-carboxyfluorescein (BCECF). J. Immunol. Methods 108: 255-264, 1988.
57. i in lethal oxidative injury in rat cultured inner medullary collecting duct cells. Pflügers Arch. 430: 697-704, 1995.
58. LACHICA, E. A., RüBSAMEN, R., ZIRPEL, L., AND RUBEL, E. W Glutamatergic inhibition of voltage-operated calcium channels in the avian cochlear nucleus. J. Neurosci. 15: 1724-1734, 1995.
59. LARMET, Y., DOLPHIN, A. C., AND DAVIES, A. M. Intracellular calcium regulates the survival of early sensory neurons before they become dependent on neurotrophic factors. Neuron 9: 563-574, 1992.
60. LEE, S., CHRISTAKOS, S., SMALL, M. B. Apoptosis and signal transduction: clues to a molecular mechanism. Curr. Opin. Cell. Biol. 5: 286-291, 1993.
61. LEGENDRE, P., ROSENMUND, C., AND WESTBROOK, G. L. Inactivation of NMDA channels in cultured hippocampal neurons by intracellular calcium. J. Neurosci. 13: 674-684, 1993.
62. LI, Y. Q., Guo, Y. P., JAY, V., STEWART, P. A., AND WONG, C. S. Time course of radiation-induced apoptosis in the adult rat spinal cord. Radiother. Oncol. 39: 35-42, 1996.
63. LIPPE, W. R. Rhythmic spontaneous activity in the developing avian auditory system. J. Neurosci. 14: 1486-1495, 1994.
64. LIZARD, G., FOURNEL, S., GENESTIER, L., DHEDIN, N., CHAPUT, C., FLACHER, M., MUTIN, M., PANAYE, G., AND REVILLARD, J. P. Kinetics of plasma membrane and mitochondrial alterations in cells undergoing apoptosis. Cytometry 21: 275-283, 1995.
65. LONDON, N. J., CONTRACTOR, H., LAKE, S. P., AUCOTT, G. C., BELL, P. R., AND JAMES, R. F. A microfluorometric viability assay for isolated human and rat islets of Langerhans. Diabetes Res. 12: 141-149, 1989.
66. LUCAS, M., SANCHEZ-MARGALET, V., SANZ, A., AND SOLANO, F. Protein kinase C activation promotes cell survival in mature lymphocytes prone to apoptosis. Biochem. Pharmacol. 47: 667-672, 1994.
67. MADISON, D. V. AND NICOLL, R. A. Cyclic adenosine 3′, 5′-monophosphate mediates B-receptor actions of noradrenaline in rat hippocampal pyramidal cells. J. Physiol. (Lond.) 372: 245-259, 1986.
68. MAIESE, K., SWIRIDUK, M., AND TENBROEKE, M. Cellular mechanisms of protection by metabotropic glutamate receptors during anoxia and nitric oxide toxicity. J. Neurochem. 66: 2419-2248, 1996.
69. MALENKA, R. C., MADISON, D. V., ANDRADE R., AND NICOLL, R. A. Phorbol esters mimic some cholincrgic actions in hippocampal pyramidal neurons. J. Neurosci. 6: 475-480, 1986.
70. 2+ influx elicited by glutamate: role in neuronal death. Mol. Pharmacol. 36: 106-112, 1989.
71. MARTIN, M. Excitatory amino acid pharmacology of the auditory nerve and nucleus magnocellularis of the chicken. Hear. Res. 17: 153-160, 1985.
72. MAYRLEITNER, M., CHANDLER, R., SCHINDLER, H., AND FLEISCHER, S. Phosphorylation with protein kinases modulates calcium loading of terminal cisternae of sarcoplsmic reticulum from skeletal muscle. Cell. Calcium 18: 197-206, 1995.
73. 2+ concentration. Arch. Biochem. Biophys. 269: 365-370, 1989.
74. MICHAELS, R. L. AND ROTHMAN, S. M. Glutamate neurotoxicity in vitro: antagonist pharmacology and intracellular calcium concentrations. J. Neurosci. 10: 283-292, 1990.
75. MILLER, R. J. Protein kinase C: a key regulator of neuronal excitability? Trends Neurosci. 9: 538-541, 1986.
76. MILLS, L, R. AND KATER, S. B. Neuron-specific and state-specific differences in calcium homeostasis regulate the generation and degeneration of neuronal architecture. Neuron 2: 149-163, 1990.
77. MISSIAEN, L., TAYLOR, C. W., AND BERRIDGE, M. J. Spontaneous calcium release from inositol trisphosphate sensitive calcium stores. Nature 352: 241-244, 1991.
78. MOORE, D. R. Developmental plasticity of the brainstem and midbrain auditory nuclei. In: Development of Auditory and Vestibular Systems 2. Amsterdam, Elsevier, 1992, p. 297-320.
79. NAKAJIMA, Y., IWAKABE, H., AKAZAWA, C., NAWA, H., SHIGEMOTO, R., MIZUNO, N., AND NAKANISHI S. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J. Biol. Chem. 268: 11868-11873, 1993.
80. NEMETH, E. F., JACKSON, H., AND PARKS, T. N. Pharmacological evidence for synaptic transmission mediated by non-N-methyl-D-aspartate receptors in the avian cochlear nucleus. Neurosci. Lett. 40: 39-44, 1983.
81. NICOLETTI, F., WROBLEWSKI, J. T., ALHO, H., EVA, C., FADDA, E., AND COSTA, E. Lesions of the putative glutamatergic pathways potentiate the increase of inositol phospholipid hydrolysis elicited by excitatory amino acids. Brain Res. 436: 103-112, 1987.
82. NICOLETTI, I., MIGLIORATI, G., PAGLIACCI, M. C., GRIGNANI, F., AND RICCARDI, C. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139: 271-279, 1991.
83. NISHIZUKA, Y. The role of protein kinase C in cell surface transduction and tumor promotion. Nature 308: 691-698, 1984.
84. NISHIZUKA, Y. Studies and perspectives of protein kinase C. Science 233: 305-311, 1986.
85. OKAMOTO, N., HORI, S., AKAZAWA, C., HAYASHI, Y., SHIGEMOTO, R., MIZUNO, N., AND NAKANISHI S. Molecular cloning of a new metabotropic glutamate receptor mGluR7 coupled to inhibitory cyclic AMP signal transduction. J. Biol. Chem. 269: 1231-1236, 1994.
86. 2+ permeability mediate synaptic transmission in the avian auditory pathway. J. Physiol. (Lond.) 482: 309-315, 1995.
87. PARKS, T. N. Changes in the length and organization of nucleus laminaris dendrites after unilateral otocyst ablation in chick embryos. J Comp Neurol 202: 47-57, 1981.
88. PARKS, T. N. AND RUBEL, E. W Organization and development of brain stem auditory nuclei of the chicken: primary afferent projections. J. Comp. Neurol. 180: 439-448, 1978.
89. RAMAN, I. M. AND TRUSSELL, L. O. The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron 9: 173-186, 1992.
90. RANDALL, R. D. AND THAYER, S. A. Glutamate-induced calcium transient triggers delayed calcium overload and neurotoxicity in rat hippocampal neurons. J. Neurosci. 12: 1881-1895, 1992.
91. ROTHMAN, S. Excitotoxins: possible mechanisms of action. Ann. NY Acad. Sci. 648: 132-139, 1992.
92. ROTHMAN, S. M. AND OLNEY, J. W. Glutamate and the pathophysiology of hypoxic-ischemic brain damage. Ann. Neurol. 19: 105-111, 1986.
93. RUBEL, E. W, HYSON, R. L., AND DURHAM, D. Afferent regulation of neurons in the brain stem auditory system. J. Neurobiol. 21: 169-196, 1990.
94. SCHOEPP, D. D. The biochemical pharmacology of metabotropic glutamate receptors. Biochem. Soc. Trans. 21: 97-102, 1993.
95. 2+ channel modulation. J. Neurophysiol. 76: 311-320, 1996.
96. SIESJÖ, B. K. Calcium and cell death. Magnesium 8: 223-237, 1989.
97. STEWARD, O. AND RUBEL, E. W Affferent influences on brain stem auditory nuclei of the chicken: Cessation of amino acid incorporation as an antecedent to age-dependent transneuronal degeneration. J. Comp. Neurol. 231: 385-395, 1985.
98. STOCLET, J.-C., GERARD, D., KILHOEFFER, M.-C., LUGNIER, C., MILLER, R., AND SCHAEFFER, P. Calmodulin and its role in calcium regulation. Prog. Neurobiol. 29: 321-364, 1987.
99. SUPPATONE, S., WORLEY, P. F, BARABAN, J. M., AND SNYDER, S. H. Solubilization, purification, and characterization of an inositol trisphosphate receptor. J. Biol. Chem. 263: 1530-1534, 1988.
100. SUZUKI, Y., YOSHIKAWA, K., AND YOKOCHI, T. A new sensitive and rapid automated fluorometric assay for detection of natural killer activity using carboxyfluorescein diacetate. J. Immunoassay 12: 145-157, 1991.
101. 2+ channels by protein kinase C in rat central and peripheral neurons: disruption of G protein-mediated inhibition. Neuron 11: 305-320, 1993.
102. TANABE, Y., MASU, M., ISII, T., SHIGEMOTO, R., NAKANISHI, S. A family of metabotropic glutamate receptors. Neuron 8: 169-179, 1992.
103. TAYLOR, C. W. AND MARSHALL, I. C. B. Calcium and inositol-1,4,5-trisphosphate receptors: a complex relationship. Trends Biochem. Sci. 17: 403-407, 1992.
104. THOMPSON, A. K., MOSTAFAPOUR, S. P., DENLINGER, L. C., BLEASDALE, J. E., AND FISHER. S. K. The aminosteroid U-73122 inhibits muscarinic receptor sequestration and phosphoinositide hydrolysis in SK-N-SH neuroblastoma cells. J. Biol. Chem. 266: 23856-23862, 1991.
105. TOULLEC. D., PIANETTI, P., COSTE, H., BELLEVERGLE, P., GRAND-PERRETT, T., AJAKANES, M., BAUDET, V., BOISSIN, P., BOURSIER, E., LORIOLLE, F., DUHAMEL, L., CHARON, D., AND KIRILOVSKY J. The bisindolymaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266: 15771-15781, 1991.
106. TYMIANSKI, M., CHARLTON, M. P., CARLEN, P. L., AND TATOR, C. H. Source specificity of early calcium neurotoxicity in cultured embryonic spinal neurons. J. Neurosci. 13: 2085-2104, 1993.
107. 2+ release II. Effect of cAMP-dependent protein kinase. Am. J. Physiol. 258 (Cell Physiol. 27): C1086-C1091, 1990.
108. VORNOV, J. J., TASKER, R. C., AND COYLE, J. T. Direct observation of the agonist-specific regional vulnerability to glutamate, NMDA, and kainate neurotoxicity in organotypic hippocampal cultures. Exp. Neurol. 114: 11-22, 1991.
109. VYKLICKY, L. J. Calcium-mediated modulation of N-methyl-D-aspartate (NMDA) responses in cultured rat hippocampal neurons. J. Physiol. (Lond.) 470: 575-600, 1993.
110. + and phorbol ester activate protein kinase C and support the survival of chick sympathetic neurons in culture. J. Neurochem. 51: 975-983, 1988.
111. WANG, L.-Y., SALTER, M. W., AND MACDONALD J. F. Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253: 1132-1135, 1991.
112. WARCHOL, M. E. AND DALLOS P. Neural coding in the chick cochlear nucleus. J. Comp. Physiol. [A] 166: 721-734, 1990.
113. WESTERBERG, B. D. AND SCHWARZ, D.W.F. Connections of the superior olive in the chicken. J. Otolaryngol. 24: 20-30, 1995.
114. WIESEL, T. N. AND HUBEL, D. H. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J. Neurophysiol. 26: 978-993, 1963a.
115. WIESEL, T. N. AND HUBEL, D. H. Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26: 1003-1017, 1963b.
116. WILDE, G.J.C., SUNDSTROM, L. E., AND IANOTTI, F. Propidium iodide in vivo: an early marker of neuronal damage in rat hippocampus. Neurosci. Letters 180: 223-226, 1994.
117. WOOLF, N. K., SHARP, F. R., DAVIDSON, T. M., AND RYAN, A. F. Cochlear and middle ear effects on metabolism in the central auditory pathway during silence: a 2-deoxyglucose study. Brain Res. 274: 119-127, 1983.
118. WYLLIE, A. H., MORRIS, R. G., SMITH, A. L., AND DUNLOP, D. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142: 67-77, 1984.
119. ZHOU, N. AND PARKS, T. N. Developmental changes in the effects of drugs acting at NMDA or non-NMDA receptors on synaptic transmission in the chick cochlear nucleus (nuc. magnocellularis). Dev. Brain Res. 67: 145-152, 1992a.
120. ZHOU, N. AND PARKS, T. N. γ-D-glutamylaminomethyl sulfonic acid (GAMS) distinguishes subtypes of glutamate receptors in the chick cochlear nucleus (nuc. magnocellularis). Hear. Res. 60: 20-26, 1992b.
121. ZHOU, N., TAYLOR, D. A., AND PARKS, T. N. Cobalt-permeable non-NMDA receptors in developing chick brainstem auditory nuclei. Neuroreport 6: 2273-2276, 1995.
122. ZIRPEL, L., LACHICA, E. A., AND LIPPE, W. R. Deafferentation increases the intracellular calcium of cochlear nucleus neurons in the embryonic chick. J. Neurophysiol. 74: 1355-1357, 1995a.
123. ZIRPEL, L., LACHICA, E. A., AND RUBEL, E. W Activation of a metabotropic glutamate receptor increases intracellular calcium concentrations in neurons of the avian cochlear nucleus. J. Neurosci. 15: 214-222, 1995b.
124. ZIRPEL, L., LACHICA, E. A., AND RUBEL, E. W Afferent regulation of neurons in the avian cochlear nucleus: intracellular mechanisms and signal transduction pathways. In: Neurotransmission and Hearing Loss: Basic Science, Diagnosis and Management, San Diego, CA: Singular Publishing Group, 1997, p. 47-76.
125. ZIRPEL, L., NATHANSON, N. M., RUBEL, E. W, AND HYSON, R. L. Glutamate stimulated phosphatidylinositol metabolism in the avian cochlear nucleus. Neurosci. Lett. 168: 163-168, 1994.
126. ZIRPEL, L., AND RUBEL, E. W Eighth nerve activity regulates the intracellular calcium concentration of avian cochlear nucleus neurons via a metabotropic glutamate receptor. J. Neurophysiol. 76: 4127-4139, 1996a.
127. i in Avian Cochlear Nucleus Neurons. Soc. Neurosci. Abstr. 22: 401, 1996b.
128. ZONG, X. AND Lux, H. D. Augmentation of calcium channel currents in response to G-protein activation by GTPγS in chick sensory neurons. J. Neurosci. 14: 4847-4853, 1994.