Glutamatergic calcium responses in the developing lateral superior olive: Receptor types and their specific activation by synaptic activity patterns

Journal of Neurophysiology

Volumn 90, Issue 4, 2003, Pages 2581-2591

  Ene, F Aura ^a   Kullmann, Paul H M ^a   Gillespie, Deda C ^a   Kandler, Karl ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 2 AMINO 4 PHOSPHONOBUTYRIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 3,5 DIHYDROXYPHENYLGLYCINE; 4 CARBOXY 3 HYDROXYPHENYLGLYCINE; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; ALPHA METHYL 4 CARBOXYPHENYLGLYCINE; AMPA RECEPTOR; BICUCULLINE; FURA 2; GLUTAMATE RECEPTOR; IONOTROPIC RECEPTOR; KAINIC ACID; KAINIC ACID RECEPTOR AGONIST; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NIFEDIPINE; OMEGA AGATOXIN; STRYCHNINE;

AMPLITUDE MODULATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL MATURATION; CELL SURVIVAL; CHANNEL GATING; COCHLEAR NUCLEUS; CONTROLLED STUDY; FEMALE; FREQUENCY MODULATION; HEARING ACUITY; MALE; MOLECULAR DYNAMICS; MOUSE; NEWBORN; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL; RECEPTOR UPREGULATION; SOUND DETECTION; SYNAPSE; TISSUE SLICE;

AFFERENT PATHWAYS; ANIMALS; ANIMALS, NEWBORN; CALCIUM; FEMALE; MALE; MICE; MICE, INBRED C57BL; OLIVARY NUCLEUS; RECEPTORS, GLUTAMATE; SYNAPSES;

EID: 0142026995     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00238.2003     Document Type: Article

References (96)

1. Baude A, Nusser Z, Roberts JD, Mulvihill E, McIlhinney RA, and Somogyi P. The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11: 771-787, 1993.
2. Berridge MJ. Neuronal calcium signaling. Neuron 21: 13-26, 1998.
3. Betz WJ and Bewick GS. Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. J Physiol 460: 287-309, 1993.
4. Bilak SR and Morest DK. Differential expression of the metabotropic glutamate receptor mGluR1 alpha by neurons and axons in the cochlear nucleus: in situ hybridization and immunohistochemistry. Synapse 28: 251-270, 1998.
5. Borgdorff AJ and Choquet D. Regulation of AMPA receptor lateral movements. Nature 417: 649-653, 2002.
6. Boudreau JC and Tsuchitani C. Cat superior olive S-segment cell discharge to tonal stimulation. Contrib Sens Physiol 4: 143-213, 1970.
7. Burnashev N, Zhou Z, Neher E, and Sakmann B. Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA, and kainate receptor subtypes. J Physiol 485: 403-418, 1995.
8. Caicedo A and Eybalin M. Glutamate receptor phenotypes in the auditory brainstem and mid-brain of the developing rat. Eur J Neurosci 11: 51-74, 1999.
9. 2+ permeability of glutamate receptors. Eur J Neurosci 10: 941-954, 1998.
10. Caird D and Klinke R. Processing of binaural stimuli by cat superior olivary complex neurons. Exp Brain Res 52: 385-399, 1983.
11. Caspary DM and Faingold CL. Non-N-methyl-D-aspartate receptors may mediate ipsilateral excitation at lateral superior olivary synapses. Brain Res 503: 83-90, 1989.
12. Clapham DE, Runnels LW, and Strubing C. The TRP ion channel family. Nat Rev Neurosci 2: 387-396, 2001.
13. Conn PJ and Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37: 205-237, 1997.
14. Crepel V, Aniksztejn L, Ben Ari Y, and Hammond C. Glutamate metabotropic receptors increase a Ca(2+)-activated nonspecific cationic current in CA1 hippocampal neurons. J Neurophysiol 72: 1561-1569, 1994.
15. DeVries SH and Schwartz EA. Kainate receptors mediate synaptic transmission between cones and "off" bipolar cells in a mammalian retina. Nature 397: 157-160, 1999.
16. Elezgarai I, Benitez R, Mateos JM, Lazaro E, Osorio A, Azkue JJ, Bilbao A, Lingenhoehl K, Van Der PH, Hampson DR, Kuhn R, Knopfel T, and Grandes P. Developmental expression of the group III metabotropic glutamate receptor mGluR4a in the medial nucleus of the trapezoid body of the rat. J Comp Neurol 411: 431-440, 1999.
17. Elezgarai I, Bilbao A, Mateos JM, Azkue JJ, Benitez R, Osorio A, Diez J, Puente N, Donate-Oliver F, and Grandes P. Group II metabotropic glutamate receptors are differentially expressed in the medial nucleus of the trapezoid body in the developing and adult rat. Neuroscience 104: 487-498, 2001.
18. Franklin JL and Johnson EM. Suppression of programmed neuronal death by sustained elevation of cytoplasmic calcium. Trends Neurosci 15: 501-508, 1992.
19. Frerking M, Malenka RC, and Nicoll RA. Synaptic activation of kainate receptors on hippocampal interneurons. Nat Neurosci 1: 479-486, 1998.
20. Frerking M and Nicoll RA. Synaptic kainate receptors. Curr Opin Neurobiol 10: 342-351, 2000.
21. Gabriele ML, Brunso-Bechtold JK, and Henkel CK. Plasticity in the development of afferent patterns in the inferior colliculus of the rat after unilateral cochlear ablation. J Neurosci 20: 6939-6949, 2000.
22. Glowatzki E and Fuchs PA. Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 288: 2366-2368, 2000.
23. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
24. Gu X, Olson EC, and Spitzer NC. Spontaneous neuronal calcium spikes and waves during early differentiation. J Neurosci 14: 6325-6335, 1994.
25. Gummer AW and Mark RF. Patterned neural activity in brain stem auditory areas of a prehearing mammal, the tammar wallaby (Macropus eugenii). Neuroreport 5: 685-688, 1994.
26. Hayashi Y, Sekiyama N, Nakanishi S, Jane DE, Sunter DC, Birse EF, Udvarhelyi PM, and Watkins JC. Analysis of agonist and antagonist activities of phenylglycine derivatives for different cloned metabotropic glutamate receptor subtypes. J Neurosci 14: 3370-3377, 1994.
27. Helfert RH and Schwartz IR. Morphological features of five neuronal classes in the gerbil lateral superior olive. Am J Anat 179: 55-69, 1987.
28. 2+ permeability of KAAMPA-gated glutamate receptor channels depends on subunit composition. Science 252: 851-853, 1991.
29. Huang EP. Synaptic transmission: spillover at central synapses. Curr Biol 8: R613-R615, 1998.
30. Isaacson JS. Spillover in the spotlight. Curr Biol 10: R475-R477, 2000.
31. Ito I, Kohda A, Tanabe S, Hirose E, Hayashi M, Mitsunaga S, and Sugiyama H. 3, 5-Dihydroxyphenyl-glycine: a potent agonist of metabotropic glutamate receptors. Neuroreport 3: 1013-1016, 1992.
32. Jaarsma D, Dino MR, Ohishi H, Shigemoto R, and Mugnaini E. Metabotropic glutamate receptors are associated with non-synaptic appendages of unipolar brush cells in rat cerebellar cortex and cochlear nuclear complex. J Neurocytol 27: 303-327, 1998.
33. Jia Z, Agopyan N, Miu P, Xiong Z, Henderson J, Gerlai R, Taverna FA, Velumian A, MacDonald J, Carlen P, Abramow-Newerly W, and Roder J. Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17: 945-956, 1996.
34. Jones SJ and Perez N. The auditory "C-process": analyzing the spectral envelope of complex sounds. Clin Neurophysiol 112: 965-975, 2001.
35. Kandler K and Friauf E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brain stem of perinatal rats. J Neurosci 15: 6890-6904, 1995.
36. 2+] with fluorescent indicators. Methods Cell Biol 40: 155-181, 1994.
37. Keele NB, Neugebauer V, and Shinnick-Gallagher P. Differential effects of metabotropic glutamate receptor antagonists on bursting activity in the amygdala. J Neurophysiol 81: 2056-2065, 1999.
38. Kidd FL and Isaac JT. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400: 569-573, 1999.
39. Kim CH, Chung HJ, Lee HK, and Huganir RL. Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc Natl Acad Sci USA 98: 11725-11730, 2001.
40. Kim G and Kandler K. Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6: 282-290, 2003.
41. Kitzes LM, Kageyama GH, Semple MN, and Kil J. Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea. J Comp Neurol 353: 341-363, 1995.
42. Kotak VC and Sanes DH. Synaptically evoked prolonged depolarizations in the developing auditory system. J Neurophysiol 74: 1611-1620, 1995.
43. Kotak VC and Sanes DH. Developmental influence of glycinergic transmission: regulation of NMDA receptor-mediated EPSPs. J Neurosci 16: 1836-1843, 1996.
44. Kotak VC and Sanes DH. Deafferentation weakens excitatory synapses in the developing central auditory system. Eur J Neurosci 9: 2340-2347, 1997.
45. Kros CJ, Ruppersberg JP, and Rusch A. Expression of a potassium current in inner hair cells during development of hearing in mice. Nature 394: 281-284, 1998.
46. Kullmann PH, Ene FA, and Kandler K. Glycinergic and GABAergic calcium responses in the developing lateral superior olive. Eur J Neurosci 15: 1093-1104, 2002.
47. 2+]i in avian cochlear nucleus neurons. J Neurobiol 37: 321-337, 1998.
48. Lachica EA, Rubsamen R, Zirpel L, and Rubel EW. Glutamatergic inhibition of voltage-operated calcium channels in the avian cochlear nucleus. J Neurosci 15: 1724-1734, 1995.
49. Lawrence JJ and Trussell LO. Long-term specification of AMPA receptor properties after synapse formation. J Neurosci 20: 4864-4870, 2000.
50. 2+ permeability. J Neurosci 21: 4572-4581, 2001.
51. Lippe WR. Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14: 1486-1495, 1994.
52. Lohmann C, Ilic V, and Friauf E. Development of a topographically organized auditory network in slice culture is calcium dependent. J Neurobiol 34: 97-112, 1998.
53. Lohrke S and Friauf E. Developmental distribution of the glutamate receptor subunits KA2, GluR6/7, and delta 1/2 in the rat medial nucleus of the trapezoid body. A quantitative image analysis. Cell Tissue Res 308: 19-33, 2002.
54. Magee J, Hoffman D, Colbert C, and Johnston D. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu Rev Physiol 60: 327-346, 1998.
55. Maiese K, Ahmad I, TenBroeke M, and Gallant J. Metabotropic glutamate receptor subtypes independently modulate neuronal intracellular calcium. J Neurosci Res 55: 472-485, 1999.
56. Man HY, Lin JW, Ju WH, Ahmadian G, Liu L, Becker LE, Sheng M, and Wang YT. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25: 649-662, 2000.
57. Mayer ML, Westbrook GL, and Guthrie PB. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurons. Nature 309: 261-263, 1984.
58. Molitor SC and Manis PB. Evidence for functional metabotropic glutamate receptors in the dorsal cochlear nucleus. J Neurophysiol 77: 1889-1905, 1997.
59. Moore DR. Trophic influences of excitatory and inhibitory synapses on neurones in the auditory brain stem. Neuroreport 3: 269-272, 1992.
60. 2+-Responses in Developing LSO Neurons. Assoc. Res. Otolaryngol. Abs 25: 184, 2002.
61. Nowak L, Bregestovski P, Ascher P, Herbet A, and Prochiantz A. Magnesium gates glutamate-activated channels in mouse central neurons. Nature 307: 462-465, 1984.
62. Oertel D. The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61: 497-519, 1999.
63. Ollo C and Schwartz IR. The superior olivary complex in C57BL/6 mice. Am J Anat 15: 349-374, 1979.
64. Otani S, Daniel H, Takita M, and Crepel F. Long-term depression induced by postsynaptic group II metabotropic glutamate receptors linked to phospholipase C and intracellular calcium rises in rat prefrontal cortex. J Neurosci 22: 3434-3444, 2002.
65. Peterlin ZA, Kozloski J, Mao BQ, Tsiola A, and Yuste R. Optical probing of neuronal circuits with calcium indicators. Proc Natl Acad Sci USA 97: 3619-3624, 2000.
66. Petralia RS, Rubio ME, Wang YX, and Wenthold RJ. Differential distribution of glutamate receptors in the cochlear nuclei. Hear Res 147: 59-69, 2000.
67. Petralia RS, Wang YX, Singh S, Wu C, Shi L, Wei J, and Wenthold RJ. A monoclonal antibody shows discrete cellular and subcellular localizations of mGluR1 alpha metabotropic glutamate receptors. J Chem Neuroanat 13: 77-93, 1997.
68. Petralia RS, Wang YX, and Wenthold RJ. 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, 1994.
69. Petralia RS, Wang YX, Zhao HM, and Wenthold RJ. Ionotropic and metabotropic glutamate receptors show unique postsynaptic, presynaptic, and glial localizations in the dorsal cochlear nucleus. J Comp Neurol 372: 356-383, 1996.
70. Pin JP and Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34: 1-26, 1995.
71. Rietzel HJ and Friauf E. Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J Comp Neurol 390: 20-40, 1998.
72. Romand R and Ehret G. Development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice. Brain Res Dev Brain Res 54: 221-234, 1990.
73. Russell FA and Moore DR. Afferent reorganisation within the superior olivary complex of the gerbil: development and induction by neonatal, unilateral cochlear removal. J Comp Neurol 352: 607-625, 1995.
74. Sanes DH and Friauf E. Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res 147: 46-58, 2000.
75. Sanes DH and Rubel EW. The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J Neurosci 8: 682-700, 1988.
76. Sato K, Nakagawa H, Kuriyama H, and Altschuler RA. Differential distribution of N-methyl-D-aspartate receptor-2 subunit messenger RNA in the rat superior olivary complex. Neuroscience 89: 839-853, 1999.
77. 2+ concentrations. Chem Biol 3: 765-774, 1996.
78. Schwartz IR and Eager PR. Glutamate receptor subunits in neuronal populations of the gerbil lateral superior olive. Hear Res 137: 77-90, 1999.
79. Spitzer NC, Lautermilch NJ, Smith RD, and Gomez TM. Coding of neuronal differentiation by calcium transients. Bioessays 22: 811-817, 2000.
80. Stellwagen D and Shatz CJ. An instructive role for retinal waves in the development of retinogeniculate connectivity. Neuron 33: 357-367, 2002.
81. Sugden SG, Zirpel L, Dietrich CJ, and Parks TN. Development of the specialized AMPA receptors of auditory neurons. J Neurobiol 52: 189-202, 2002.
82. Takahashi T, Forsythe ID, Tsujimoto T, Barnes-Davies M, and Onodera K. Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274: 594-597, 1996.
83. Takumi Y, Matsubara A, Rinvik E, and Ottersen OP. The arrangement of glutamate receptors in excitatory synapses. Ann NY Acad Sci 868: 474-482, 1999.
84. Tanabe Y, Nomura A, Masu M, Shigemoto R, Mizuno N, and Nakanishi S. Signal transduction, pharmacological properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4. J Neurosci 13: 1372-1378, 1993.
85. Thompson AM and Schofield BR. Afferent projections of the superior olivary complex. Microsc Res Tech 51: 330-354, 2000.
86. Verdoorn TA, Burnashev N, Monyer H, Seeburg PH, and Sakmann B. Structural determinants of ion flow through recombinant glutamate receptor channels. Science 252: 1715-1718, 1991.
87. Vitten H, Friauf E, Peich L, and Lohrke S. Kainate mediated currents in lateral superior olive neurons of the rat. Soc Neurosci Abstr 25 (part 1): 392.16, 1999.
88. Vizi ES, Mike A, and Tarnawa I. The functional study of kainate receptors - hopes and doubts. Trends Neurosci 20: 396-397, 1997.
89. West AE, Griffith EC, and Greenberg ME. Regulation of transcription factors by neuronal activity. Nat Rev Neurosci 3: 921-931, 2002.
90. Wong RO and Ghosh A. Activity-dependent regulation of dendritic growth and patterning. Nat Rev Neurosci 3: 803-812, 2002.
91. Wu SH and Fu XW. Glutamate receptors underlying excitatory synaptic transmission in the rat's lateral superior olive studied in vitro. Hear Res 122: 47-59, 1998.
92. Wu SH and Kelly JB. Synaptic pharmacology of the superior olivary complex studied in mouse brain slice. J Neurosci 12: 3084-3097, 1992.
93. Zhang LI, Tao HW, and Poo M. Visual input induces long-term potentiation of developing retinotectal synapses. Nat Neurosci 3: 708-715, 2000.
94. Zirpel L, Janowiak MA, Taylor DA, and Parks TN. Developmental changes in metabotropic glutamate receptor-mediated calcium homeostasis. J Comp Neurol 421: 95-106, 2000.
95. 2+]i in avian cochlear nucleus neurons: roles of protein kinases A and C and relation to cell death. J Neurophysiol 79: 2288-2302, 1998.
96. Zirpel L and Rubel EW. Eighth nerve activity regulates intracellular calcium concentration of avian cochlear nucleus neurons via a metabotropic glutamate receptor. J Neurophysiol 76: 4127-4139, 1996.