Glutamatergic and GABAergic agonists increase [Ca2+](i) in avian cochlear nucleus neurons

Journal of Neurobiology

Volumn 37, Issue 2, 1998, Pages 321-337

  Lachica, E A ^a   Kato, B Maya ^a   Lippe, W R ^a   Rubel, Edwin W ^a  

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

Author keywords

Auditory system; Fura 2; Glutamate receptors; Nucleus magnocellularis; Second messengers

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 1 (5 ISOQUINOLINESULFONYL) 2 METHYLPIPERAZINE; 1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; 1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 3,4,5 TRIMETHOXYBENZOIC ACID 8 (DIETHYLAMINO)OCTYL ESTER; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AZETIDINE DERIVATIVE; CALCIUM; CALCIUM CHANNEL BLOCKING AGENT; CYSTEINE SULFINIC ACID; EGTAZIC ACID; FORSKOLIN; FURA 2; GLUTAMATE RECEPTOR AGONIST; GLUTAMIC ACID; GLYCINE; IBOTENIC ACID; KAINIC ACID; METABOTROPIC RECEPTOR; N (2 METHYLAMINOETHYL) 5 ISOQUINOLINESULFONAMIDE; N METHYL DEXTRO ASPARTIC ACID; NIFEDIPINE; PHORBOL 13 ACETATE 12 MYRISTATE; SPERMIDINE; THAPSIGARGIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; BRAIN STEM; CALCIUM CELL LEVEL; CHICKEN; COCHLEAR NUCLEUS; CONTROLLED STUDY; GABAERGIC SYSTEM; MAGNOCELLULAR NUCLEUS; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SUPERIOR OLIVARY NUCLEUS;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CALCIUM; CHICK EMBRYO; COCHLEAR NUCLEUS; EXCITATORY AMINO ACID AGONISTS; FLUORESCENT DYES; FURA-2; GABA AGONISTS; KAINIC ACID; N-METHYLASPARTATE; NEURONS; STIMULATION, CHEMICAL;

EID: 0031724212     PISSN: 00223034     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4695(19981105)37:2<321::AID-NEU10>3.0.CO;2-M     Document Type: Article

References (112)

1. ARAMORI, I., and NAKANISHI, S. (1992). Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8:757-765.
2. BEN-ARI, Y., TSEEB, V., RAGGOZZINO, D., KHAZIPOV, R., and GAIARSA, J. L. (1994). Gamma-aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog. Brain Res. 102:261-273.
3. BERNINGER, B., MARTY, S., ZAFRA, F., DA-PENHA-BERZAGHI, M., THOENEN, H., and LINDHOLM, D. (1995). GABAergic stimulation switches from enhancing to repressing BDNF expression in rat hippocampal neurons during maturation in vitro. Development 121:2327-2335.
4. BOORD, R. L. (1969). The anatomy of the avian auditory system. Ann. NY Acad. Sci. 167:147-155.
5. Boss, V., and CONN, P. J. (1992). Metabotropic excitatory amino acid receptor activation stimulates phospholipase D in hippocampal slices. J. Neurochem. 59:2340-2343.
6. Boss, V., and BOATEN, A. S. (1995). An L-cysteine sulfinic acid-sensitive metabotropic receptor mediates increased cAMP accumulation in hippocampal slices. Neurosci. Lett. 184:1-4.
7. Boss, V., NUTT, K. M., and CONN, P. J. (1994). L-cysteine sulfinic acid as an endogenous agonist of a novel metabotropic receptor coupled to stimulation of phospholipase D activity. Mol. Pharmacol. 45:1177-1182.
8. BRENOWITZ, S., and TRUSSELL, L. (1997). Enhancements of synaptic strength through activation of presynaptic GABA-B receptors. Soc. Neurosci. Abstr. 23:365.
9. CARBONE, E., and SWANDULLA, D. (1989). Neuronal calcium channels: kinetics, blockade and modulation. Prog. Biophys. Mol. Biol. 54:31-58.
10. CHAPMAN, A. G., MELDRUM, B. S., and SIESJO, B. K. (1977). Cerebral metabolic changes during prolonged epileptic seizures in rats. J. Neurochem. 28:1025-1035.
11. CHEN, Q., HARRIS, C., BROWN, C. S., HOWE, A., SURMEIER, D. J., and REINER, A. (1995). Glutamate-mediated excitotoxic death of cultured striatal neurons is mediated by non-NMDA receptors. Exp. Neurol. 136:212-224.
12. CHESLER, M. (1990). The regulation and modulation of pH in the nervous system. Prog. Neurobiol. 34:401-427.
13. CHESLER, M., and KAILA, K. (1992). Modulation of pH by neuronal activity. Trends Neurosci. 5:396-402.
14. CHIOU, G. C., and HONG, S. J. (1995). Prevention and reduction of neural damage in ischemic strokes by w-(N.N′-diethylamino)-n-alkyl-3,4,5-trimethoxybenzoate compounds. J. Pharmacol. Exp. Ther. 275:474-478.
15. CHUNG, D. S., WINDER, D. G., and CONN, P. J. (1994). 4-Bromohomoibotenic acid selectively activates a 1-aminocyclopentane-1S,3R-dicarboxylic acid-insensitive metabotropic glutamate receptor coupled to phosphoinositide hydrolysis in rat cortical slices. J. Neurochem. 63:133-139.
16. CODE, R. A., BURD, G. D., and RUBEL, E. W. (1989). Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J. Comp. Neurol. 284:504-518.
17. DESAI, M. A., BURNETT, J. P., ORNSTEIN, P. L., and SCHOEPP, D. D. (1995). Cyclothiazide acts at a site on the alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor complex that does not recognize competitive or noncompetitive AMPA receptor antagonists. J. Pharmacol. Exp. Ther. 272:38-43.
18. DONEVAN, S. D., and ROGAWSKI, M. A. (1993). GYKI 52466, a 2,3-benzodiazepine, is a highly selective, non-competitive antagonist of AMPA/kainate receptor responses. Neuron 10:51-59.
19. DUFFY, T. E., HOWSE, D. C., and PLUM, F. (1975). Cerebral energy metabolism during experimental status epilepticus. J. Neurochem. 24:925-934.
20. 2+ exchanger in neuronal cells. Mol. Pharmacol. 43:976-981.
21. FAVARON, M., MANEV, R. M., CANDEO, P., ARBAN, R., GABELLINI, N., KOZIKOWSKI, A. P., and MANEV, H. (1993). Trans-azetidine-2,4-dicarboxylic acid activates neuronal metabotropic receptors. Neuroreport 4:967-970.
22. FERRIS, C. D., HUGANIR, R. L., BREDT, D. S., CAMERON, A. M., and SYNDER, S. H. (1991). 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.
23. GAIARSA, J. L., MCLEAN, H., CONGAR, P., LEINEKUGEL, X., KHAZIPOV, R., TSEEB, V., and BEN-ARI, Y. (1995). Postnatal maturation of gamma-aminobutyric acid A and B-mediated inhibition in the CA3 hippocampal region of the rat. J. Neurobiol. 26:339-349.
24. GILBERTSON, T. A., SCOBEY, R., and WILSON, M. (1991). Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells. Science 251:1613-1615.
25. 2+ antagonist in cultured mouse coritcal neurones. Neuroreport 5:605-608.
26. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440-3450.
27. 2+ influx studies. J. Neurochem. 65:1077-1084.
28. HAMBURGER, V., and HAMILTON, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88:49-92.
29. HERB, A., BURNASHEV, N., WERNER, P., SAKMANN, B., WISDEN, W., and SEEBURG, P. H. (1992). The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8:775-785.
30. HOLLER, T., CAPPEL, E., KLEIN, J., and LOFFELHOLZ, K. (1993). Glutamate activates phospholipase D in hippocampal slices of newborn and adult rats. J. Neurochem. 61:1569-1572.
31. HYSON, R. L., and SADLER, K. A. (1997). Differences in expression of GABA receptor subunits, but not benzodiazepine binding in the chick brain stem auditory system. J. Mol. Neurosci. 8:193-205.
32. HYSON, R. L., REYES, A. D., and RUBEL, E. W. (1995). A depolarizing inhibitory response to GABA in brain stem auditory neurons of the chick. Brain Res. 677:117-126.
33. IINO, M., OZAWA, S., and TSUZUKI, K. (1990). Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones. J. Physiol. Lond. 424:151-165.
34. JHAVERI, S., and MOREST, D. K. (1982a). Neuronal architecture in nucleus magnocellularis of the chicken auditory system with observation on nucleus laminaris: a light and electron microscope study. Neuroscience 7:809-836.
35. JHAVERI, S., and MOREST, D. K. (1982b). Sequential alterations of neuronal architecture in nucleus magnocellularis of the developing chicken: a Golgi study. Neuroscience 7:837-853.
36. 2+ stores in brainstem auditory neurons. J. Neurophysiol. 76:646-650.
37. KATO, B. M., and RUBEL, E. W. (1998). Glutamate regulates IP3-type and CICR stores in the avian cochlear nucleus. J. Neurophysiol. (submitted).
38. KOZIKOWSKI, A. P., TUCKMANTEL, W., LIAO, Y., MANEV, H., IKONOMOVIC, S., and WROBLEWSKI, J. T. (1993). Synthesis and metabotropic receptor activity of the novel rigidified glutamate analogues (+)- and (-)-trans-azetidine-2,4-dicarboxylic acid and their N-methyl derivatives. J. Med. Chem. 36:2706-2708.
39. KRISHTAL, O. A., OSIPCHUK, Y. V., SHELEST, T. N., and SMIRNOFF, S. V. (1987). Rapid extracellular pH transients related to synaptic transmission in rat hippocampal slices. Brain Res. 436:352-356.
40. LACHICA, E. A., RÜBSAMEN, R., and RUBEL, E. W. (1994). GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus. J. Comp. Neurol. 348:403-418.
41. LACHICA, E. A., RÜBSAMEN, R., ZIRPEL, L., and RUBEL, E. W. (1995). Glutamatergic inhibition of voltage-operated calcium channels in the avian cochlear nucleus. J. Neurosci. 15:1724-1734.
42. LACHICA, E. A., ZIRPEL, L., and RUBEL, E. W. (1996). Intracellular mechanisms involved in the afferent regulation of neurons in the avian cochlear nucleus. In: Auditory System Plasticity and Regeneration. R. J. Salvi, D. Henderson, F. Fiorini, and V. Colletti, Eds. Thieme Medical Publishers, New York, pp. 333-353.
43. LEINDERS-ZUFALL, T., ROSENBOOM, H., BARNSTABLE, C. J., SHEPHERD, G. M., and ZUFALL, F. (1995). A calcium-permeable cGMP-activated cation conductance in hippocampal neurons. Neuroreport 6:1761-1765.
44. 2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J. Physiol. Lond. 487:319-329.
45. LERMA, J., PATERNAIN, A. V., NARANJO, J. R., and MELLSTROM, B. (1993). Functional kainate-selective glutamate receptors in cultured hippocampal neurons. Proc. Natl. Acad. Sci. USA 90:11688-11692.
46. LU, T., OERTEL, D., and TRUSSELL, L. (1997). GABA-evoked conductance in the avian cochlear nucleus. Soc. Neurosci. Abstr. 23:1548.
47. MATTHEWS, G., AYOUB, G. S., and HEIDELBERGER, R. (1994). Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology. J. Neurosci. 14:1079-1090.
48. MCBAIN, C. J., and MAYER, M. L. (1994). N-methyl-D-aspartic acid receptor structure and function. Physiol. Rev. 74:723-760.
49. ++ influx into striatal neurons by kainic acid. J. Pharmacol. Exp. Ther. 249:184-193.
50. MURPHY, S. N., THAYER, S. A., and MILLER, R. J. (1987). The effects of excitatory amino acids on intracellular calcium in single mouse striatal neurons in vitro. J. Neurosci. 7:4145-4158.
51. MUTCH, W. A., and HANSEN, A. J. (1984). Extracellular pH changes during spreading depression and cerebral ischemia: mechanisms of brain pH regulation. J. Cereb. Blood Flow. Metab. 4:17-27.
52. 3H]NS 257, a novel competitive AMPA receptor antagonist, to rat brain membranes and brain sections. J. Neurochem. 65:1264-1273.
53. 2+ transients in astrocytes. Neuroscience 54:605-614.
54. NOWYCKY, M. C., Fox, A. P., and TSEIN, R. W. (1985). Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316:440-443.
55. 2+ elevating to depressing. J. Neurosci. 15:5065-5077.
56. OBRIETAN, K., and VAN DEN POL, A. N. (1996). Growth cone calcium elevation by GABA. J. Comp. Neurol. 372:167-175.
57. OKADA, D. (1992). Two pathways of cyclic GMP production through glutamate receptor-mediated nitric oxide synthesis. J. Neurochem. 59:1203-1210.
58. 2+ permeability mediate synaptic transmission in the avian auditory pathway. J. Physiol. Lond. 482:309-315.
59. PAN, Z. H., and LIPTON, S. A. (1995). Multiple GABA receptor subtypes mediate inhibition of calcium influx at rat retinal bipolar cell terminals. J. Neurosci. 15:2668-2679.
60. PARKS, T. N. (1981). Morphology of axosomatic endings in the avian cochlear nucleus: nucleus magnocellularis of the chicken. J. Comp. Neurol. 203:425-440.
61. PARKS, T. N., and RUBEL, E. W. (1978). Organization and development of the brain stem auditory nuclei of the chicken: primary afferent projections. J. Comp. Neurol. 180:439-448.
62. PARRAM'ON, M., GONZALEZ, M. P., HERRERO, M. T., and OSET-GASQUE, M. J. (1995). GABAB receptors increase intracellular calcium concentration in chromaffin cells through two different pathways: their role in catecholamine secretion. J. Neurosci. Res. 41:65-72.
63. PARTIN, K. M., PATNEAU, D. K., WINTERS, C. A., MAYER, M. L., and BUONANNO, A. (1993). Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11:1069-1082.
64. PATERNAIN, A. V., MORALES, M., and LERMA, J. (1995). Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons. Neuron 14:185-189.
65. 2+-permeable kainate/AMPA receptors more abundant in immature brain? Neurosci. Lett. 144:65-69.
66. PELLERIN, L., and WOLFE, L. S. (1991). Release of arachidonic acid by NMDA-receptor activation in the rat hippocampus. Neurochem. Res. 16:983-989.
67. PRUSS, R. M., AKESON, R. L., RACKE, M. M., and WILBURN, J. L. (1991). Agonist-activated cobalt uptake identifies divalent cation-permeable kainate receptors on neurons and glial cells. Neuron 7:509-518.
68. QIAN, H., and DOWLING, J. E. (1995). GABAA and GABAC receptors on hybrid bass retinal bipolar cells. J. Neurophysiol. 74:1920-1928.
69. RAMAN, I. M., and TRUSSELL, L. O. (1992). The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron 9:173-186.
70. RAMAN, I. M., and TRUSSELL, L. O. (1995). The mechanism of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor desensitization after removal of glutamate. Biophys. J. 68:137-146.
71. RENARD, A., CR'EPEL, F., and AUDINAT, E. (1995). Evidence for two types of non-NMDA receptors in rat cerebellar Purkinje cells maintained in slice cultures. Neuropharmacology 34:335-346.
72. REYES, A. D., RUBEL, E. W., and SPAIN, W. J. (1994). Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J. Neurosci. 14:5352-5364.
73. RUBEL, E. W., and PARKS, T. N. (1988). Organization and development of the avian brain-stem auditory system. In: G. M. Edelman, W. E. Gall, and W. M. Cowan, Eds. Auditory Function: Neurobiological Bases of Hearing. Wiley, New York, pp. 3-92.
74. SARRI, E., PICATOSTE, F., and CLARO, E. (1995). Histamine HI and endothelin ETB receptors mediate phospholipase D stimulation in rat brain hippocampal slices. J. Neurochem. 65:837-841.
75. SCHOEPP, D. D., and JOHNSON, B. G. (1993). Metabotropic glutamate receptor modulation of cAMP accumulation in the neonatal rat hippocampus. Neuropharmacology 32: 1359-1365.
76. SEEBURG, P. H. (1993). The TIPS/TINS lecture: the molecular biology of mammalian glutamate receptor channels. Trends Pharmacol. Sci. 14:297-303.
77. 2+ mobilization induced by amitriptyline and bradykinin in rat frontocortical neurons. J. Neurochem. 61:1748-1754.
78. SHIMIZU-SASAMATA, M., KAWASAKI-YATSUGI, S., OKADA, M., SAKAMOTO, S., YATSUGI, S., TOGOMI, J., HATANAKA, K., OHMORI, J., KOSHIYA, K., USUDA, S., and MURASE, K. (1996). YM90K: pharmacological characterization as a selective and potent alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor antagonist. J. Pharmacol. Exp. Ther. 276:84-92.
79. SIMMONS, D. D., SONG, C., and GIBONEY, P. (1994). Kainic acid stimulates uptake of divalent cations in postnatal cochlear neurons. Neuroreport 5:1433-1437.
80. SOMOGYI, P., ESHHAR, N., TEICHBERG, V. I., and ROBERTS, J. D. (1990). Subcellular localization of a putative kainate receptor in Bergmann glial cells using a monoclonal antibody in the chick and fish cerebellar cortex. Neuroscience 35:9-30.
81. STELLA, N., PELLERIN, L., and MAGISTRETTI, P. J. (1995). Modulation of the glutamate-evoked release of arachidonic acid from mouse cortical neurons: involvement of a pH-sensitive membrane phospholipase A2. J. Neurosci. 15:3307-3317.
82. SUGIYAMA, H., ITO, I., and WATANABE, M. (1989). Glutamate receptor subtypes may be classified into two major categories: a study on xenopus oocytes injected with rat brain mRNA. Neuron 3:129-132.
83. SULLIVAN, W. E., and KONISHI, M. (1984). Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl. J. Neurosci. 4:1787-1799.
84. SUPATTAPONE, S., DANOFF, S. K., THEIBERT, A., SURESH, J. K., STEINER, J., and SNYDER, S. H. (1988). Cyclic AMP-dependent phosphorylation of a brain inositol trisphosphate receptor decreases its release of calcium. Proc. Natl. Acad. Sci. USA 85:8747-8750.
85. TAN, S. E., WENTHOLD, R. J., and SODERLING, T. R. (1994). Phosphorylation of AMPA-type glutamate receptors by calcium/calmodulin-dependent protein kinase II and protein kinase C in cultured hippocampal neurons. J. Neurosci. 14:1123-1129.
86. +. Proc. Natl. Acad. Sci. USA 87:6445-6449.
87. THOMSEN, C., BAU, A., FAARUP, P., FOGED, C., KANSTRUP, A., and SUZDAK, P. D. (1994). Effects of bromohomoibotenate on metabotropic glutamate receptors. Neuroreport 5:2417-2420.
88. THORESON, W. B., and MILLER, R. F. (1994). Actions of (1S,3R)-1-aminocyclopentane-1,3-dicarboxylic acid (1S,3R-ACPD) in retinal ON bipolar cells indicate that it is an agonist at L-AP4 receptors. J. Gen. Physiol. 103: 1019-1034.
89. + sensitivity of excitatory amino acid receptor channels in rat cerebellar granule neurones. J. Physiol. 433:727-763.
90. TRAYNELIS, S. F., HARTLEY, M., and HEINEMANN, S. F. (1995). Control of proton sensitivity of the NMDA receptor by RNA splicing and polyamines. Science 268: 873-876.
91. TRUSSELL, L. O., ZHANG, S., and RAMAN, I. M. (1993). Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10:1185-1196.
92. VERDOORN, T. A., JOHANSEN, T. H., DREJER, J., and NIELSEN, E. O. (1994). Selective block of recombinant glur6 receptors by NS-102, a novel non-NMDA receptor antagonist. Eur. J. Pharmacol. 269:43-49.
93. VON BARTHELD, C. S., CODE, R. A., and RUBEL, E. W. (1989). GABAergic neurons in the brainstem auditory nuclei of the chick: distribution, morphology, and connectivity. J. Comp. Neurol. 287:470-483.
94. VYKLICK'Y, L., JR., VLACHOV'A, V., and KRUSEK, J. (1990). The effect of external pH changes on responses to excitatory amino acids in mouse hippocampal neurones. J. Physiol. Lond. 430:497-517.
95. WANG, J., and JOHNSON, K. M. (1995). Regulation of cyclic 3′,5′-adenosine monophosphate accumulation and GABA release by glutamate metabotropic and dopamine D1 receptors. J. Pharmacol. Exp. Ther. 275:877-884.
96. 2+ transients in embryonic rat dorsal horn neurons in culture. Eur. J. Neurosci. 6:1275-1280.
97. WARCHOL, M. E., and DALLOS, P. (1990). Neural coding in the chick cochlear nucleus. J. Comp. Physiol. A 166:721-734.
98. WILDING, T. J., and HUETTNER, J. E. (1995). Differential antagonism of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid-preferring and kainate-preferring receptors by 2,3-benzodiazepines. Mol. Pharmacol. 47: 582-587.
99. WINDER, D. G., and CONN, P. J. (1993). Activation of metabotropic glutamate receptors increases cAMP accumulation in hippocampus by potentiating responses to endogenous adenosine. J. Neurosci. 13:38-44.
100. WONG, L. A., and MAYER, M. L. (1993). Differential modulation by cyclothiazide and concanavalin A of desensitization at native alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid- and kainate-preferring glutamate receptors. Mol. Pharmacol. 44:504-510.
101. 2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in non-N-methyl-D-aspartate glutamate receptors. Proc. Natl. Acad. Sci. USA 92:1376-1380.
102. YAMADA, K. A., and TANG, C. M. (1993). Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. J. Neurosci. 13: 3904-3915.
103. YAMASHITA, M., and FUKUDA, Y. (1993). Calcium channels and GABA receptors in the early embryonic chick retina. J. Neurobiol. 24:1600-1614.
104. ZHANG, D., PAN, Z. H., ZHANG, X., BRIDEA, A. D., and LIPTON, S. A. (1995). Cloning of a gamma-aminobutyric acid type C receptor subunit in rat retina with a methionine residue critical for picrotoxinin channel block. Proc. Natl. Acad. Sci. USA 92:11756-11760.
105. ZHANG, S., and TRUSSELL, L. O. (1994). A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J. Neurophysiol. 72:705-718.
106. ZHOU, N., and PARKS, T. N. (1992). Developmental changes in the effects of drugs acting at NMDA or non-NMDA receptors on synaptic transmission in the chick cochlear nucleus (nuc. magnocellularis). Der. Brain Res. 67:145-152.
107. ZHOU, N., TAYLOR, D. A., and PARKS, T. N. (1995). Cobalt-permeable non-NMDA receptors in developing chick brainstem auditory nuclei. Neuroreport 6:2273-2276.
108. ZIRPEL, L., LACHICA, E. A., and LIPPE, W. R. (1996). Deafferentation increases the intracellular calcium of cochlear nucleus neurons in the embryonic chick. J. Neurophysiol. 74:1355-1357.
109. ZIRPEL, L., LACHICA, E. A., and RUBEL, E. W. (1995). Activation of a metabotropic glutamate receptor increases intracellular calcium concentrations in neurons of the avian cochlear nucleus. J. Neurosci. 15:214-222.
110. ZIRPEL, L., and RUBEL, E. W. (1996). Eighth nerve activity regulates the intracellular calcium concentration of avian cochlear nucleus neurons via a metabotopic glutamate receptor. J. Neurophys. 76:4127-4139.
111. ZIRPEL, L., NATHANSON, N. M., RUBEL, E. W., and HYSON, R. L. (1994). Glutamate-stimulated phosphatidylinositol metabolism in the avian cochlear nucleus. Neurosci. Lett. 168:163-166.
112. ZORUMSKI, C. F., YAMADA, K. A., PRICE, M. T., and OLNEY, J. W. (1993). A benzodiazepine recognition site associated with the non-NMDA glutamate receptor. Neuron 10:61-67.