Glycinergic and GABAergic calcium responses in the developing lateral superior olive

European Journal of Neuroscience

Volumn 15, Issue 7, 2002, Pages 1093-1104

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

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

Author keywords

Caged glutamate; Calcium imaging; Inhibition; Mouse; Rat

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; CALCIUM; FURA 2; GLYCINE; GLYCINE RECEPTOR; NEUROTRANSMITTER;

AGE; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SLICE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; DEPOLARIZATION; HEARING; HYPERPOLARIZATION; IMAGING; NERVE CELL; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE STIMULATION; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RAT; SECOND MESSENGER; SUPERIOR OLIVARY NUCLEUS; TONOTOPY;

ANIMALS; ANIMALS, NEWBORN; AUDITORY PATHWAYS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL DIFFERENTIATION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLYCINE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONAL PLASTICITY; OLIVARY NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA; RECEPTORS, GLYCINE; SYNAPTIC TRANSMISSION;

EID: 0036455216     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2002.01946.x     Document Type: Article

References (68)

1. Adams, J.C. & Mugnaini, E. (1990) Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hearing Res., 49, 281-298.
2. Backus, K.H., Deitmer, J.W. & Friauf, E. (1998) Glycine-activated currents are changed by coincident membrane depolarization in developing rat auditory brainstem neurones. J. Physiol. (Lond.), 507, 783-794.
3. Bean, B.P. & Mintz, I.M. (1994) Pharmacology of different types of calcium channels in rats neurons. In Peracchia, C. (ed.), Handbook of Membrane Channels: Molecular and Cellular Physiology. Academic Press, San Diego, CA, pp. 199-210.
4. Ben-Ari, Y., Cherubini, E., Corradetti, R. & Gaiarsa, J.L. (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. (Lond.), 416, 303-325.
5. A, NMDA and AMPA receptors: A developmentally regulated 'menage a trois'. Trends Neurosci., 20, 523-529.
6. Bledsoe, S.C. Jr, Snead, C.R., Helfert, R.H., Prasad, V., Wenthold, R.J. & Altschuler, R.A. (1990) 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, 189-194.
7. Bootman, M.D., Collins, T.J., Peppiatt, C.M., Prothero, L.S., MacKenzie, L., De Smet, P., Travers, M., Tovey, S.C., Seo, J.T., Berridge, M.J., Ciccolini, F. & Lipp, P. (2001) Calcium signalling - An overview. Semin. Cell Dev. Biol., 12, 3-10.
8. Boudreau, J.C. & Tsuchitani, C. (1968) Binaural interaction in the cat superior olive S segment. J. Neurophysiol., 31, 442-454.
9. Caird, D. & Klinke, R. (1983) Processing of binaural stimuli by cat superior olivary complex neurons. Exp. Brain Res., 52, 385-399.
10. Cant, N.B. (1998) Structural development of the mammalian central auditory pathways. In Rubel, E.W., Popper, A.N., Fay, R.R. (eds), Development of the Auditory System. Springer Verlag, New York, NY, pp. 315-413.
11. Caspary, D.M. & Finlayson, P.G. (1991) Superior olivary complex: Functional neuropharmacology of the principal cell types. In Altschuler, R.A., Bobbin, R.P., Clopton, B.M., Hoffman, D.W. (eds), Neurobiology of Hearing: The Central Auditory System. Raven Press, New York, NY, pp. 141-161.
12. 2+ of rat cerebellar granule cells in explant cultures. J. Neurosci., 7, 1384-1400.
13. Ehrlich, I., Ilic, V., Lohmann, C. & Friauf, E. (1998) Development of glycinergic transmission in organotypic cultures from auditory brain stem. Neuroreport, 9, 2785-2790.
14. Ehrlich, I., Lohrke, S. & Friauf, E. (1999) Shift from depolarizing to hyperpolarizing glycine action in rat auditory neurones is due to age-dependent Cl- regulation. J. Physiol. (Lond.), 520, 121-137.
15. Finlayson, P.G. & Caspary, D.M. (1989) Synaptic potentials of chinchilla lateral superior olivary neurons. Hearing Res., 38, 221-228.
16. Flint, A.C., Dammerman, R.S. & Kriegstein, A.R. (1999) Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations. Proc. Natl. Acad. Sci. USA, 96, 12144-12149.
17. Frech, M.J., Deitmer, J.W. & Backus, K.H. (1999) Intracellular chloride and calcium transients evoked by gamma- aminobutyric acid and glycine in neurons of the rat inferior colliculus. J. Neurobiol., 40, 386-396.
18. Friauf, E., Hammerschmidt, B. & Kirsch, J. (1997) Development of adult-type inhibitory glycine receptors in the central auditory system of rats. J. Comp Neurol., 385, 117-134.
19. Gao, B.X., Stricker, C. & Ziskind-Conhaim, L. (2001) Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J. Neurophysiol., 86, 492-502.
20. Givens, R.S., Jung, A., Park, C.H., Weber, J. & Bartlett, W. (1997) New photoactivated protecting groups. 7. p-hydroxyphenacyl - A phototrigger for excitatory amino acids and peptides. J. Am. Chem. Soc., 119, 8369-8370.
21. Glendenning, K.K., Masterton, R.B., Baker, B.N. & Wenthold, R.J. (1991) Acoustic chiasm III: Nature, distribution, and sources of afferents to the lateral superior olive in the cat. J. Comp. Neurol., 310, 377-400.
22. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem., 260, 3440-3450.
23. 2+ transients. Nature, 375, 784-787.
24. Gu, X. & Spitzer, N.C. (1997) Breaking the code: Regulation of neuronal differentiation by spontaneous calcium transients. Dev. Neurosci., 19, 33-41.
25. Henkel, C.K. & Brunso-Bechtold, J.K. (1991) Dendritic morphology and development in the ferret lateral superior olivary nucleus. J. Comp. Neurol., 313, 259-272.
26. Jonas, P., Bischofberger, J. & Sandkuhler, J. (1998) Corelease of two fast neurotransmitters at a central synapse. Science, 281, 419-424.
27. Kakazu, Y., Akaike, N., Komiyama, S. & Nabekura, J. (1999) Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J. Neurosci., 19, 2843-2851.
28. Kandler, K. & Friauf, E. (1995) Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J. Neurosci., 15, 6890-6904.
29. Kandler, K., Katz, L.C. & Kauer, J.A. (1998) Focal photolysis of caged glutamate produces long-term depression of hippocampal glutamate receptors. Nature Neurosci., 1, 119-123.
30. Kato, B.M. & Rubel, E.W. (1999) Glutamate regulates IP3-type and CICR stores in the avian cochlear nucleus. J. Neurophysiol., 81, 1587-1596.
31. Kawabata, S., Tsutsumi, R., Kohara, A., Yamaguchi, T., Nakanishi, S. & Okada, M. (1996) Control of calcium oscillations by phosphorylation of metabotropic glutamate receptors. Nature, 383, 89-92.
32. Kirsch, J. & Betz, H. (1998) Glycine-receptor activation is required for receptor clustering in spinal neurons. Nature, 392, 717-720.
33. Korada, S. & Schwartz, I.R. (1999) Development of GABA, glycine, and their receptors in the auditory brainstem of gerbil: A light and electron microscopic study. J. Comp Neurol., 409, 664-681.
34. Kotak, V.C., Korada, S., Schwartz, I.R. & Sanes, D.H. (1998) A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J. Neurosci., 18, 4646-4655.
35. Kotak, V.C. & Sanes, D.H. (1995) Synaptically evoked prolonged depolarizations in the developing auditory system. J. Neurophysiol., 74, 1611-1620.
36. Kotak, V.C. & Sanes, D.H. (1996) Developmental influence of glycinergic transmission: Regulation of NMDA receptor-mediated EPSPs. J. Neurosci., 16, 1836-1843.
37. Kotak, V.C. & Sanes, D.H. (2000) Long-lasting inhibitory synaptic depression is age- and calcium- dependent. J. Neurosci., 20, 5820-5826.
38. Kros, C.J., Ruppersberg, J.P. & Rusch, A. (1998) Expression of a potassium current in inner hair cells during development of hearing in mice. Nature, 394, 281-284.
39. Kuhse, J., Betz, H. & Kirsch, J. (1995) The inhibitory glycine receptor: Architecture, synaptic localization and molecular pathology of a postsynaptic ion-channel complex. Curr. Opin. Neurobiol., 5, 318-323.
40. i in developing neurons of the lateral superior olive. Soc. Neurosci. Abstr., 25, 394.
41. i in avian cochlear nucleus neurons. J. Neurobiol., 37, 321-337.
42. A and NMDA receptors in the neonatal hippocampus. Neuron, 18, 243-255.
43. 2+ rise in pyramidal cells and interneurons from rat neonatal hippocampal slices. J. Physiol. (Lond.), 487, 319-329.
44. Lippe, W.R. (1994) Rhythmic spontaneous activity in the developing avian auditory system. J. Neurosci., 14, 1486-1495.
45. Liu, S.Q. & Kaczmarek, L.K. (1998) Depolarization selectively increases the expression of the Kv3.1 potassium channel in developing inferior colliculus neurons. J. Neurosci., 18, 8758-8769.
46. Lo, Y.J., Rao, S.C. & Sanes, D.H. (1998) Modulation of calcium by inhibitory systems in the developing auditory midbrain. Neuroscience, 83, 1075-1084.
47. Lohmann, C., Ilic, V. & Friauf, E. (1998) Development of a topographically organized auditory network in slice culture is calcium dependent. J. Neurobiol., 34, 97-112.
48. 2+ concentration of hippocampal CA1 pyramidal neurons. J. Neurophysiol., 76, 3460-3470.
49. Moore, J.K. & Moore, R.Y. (1987) Glutamic acid decarboxylase-like immunoreactivity in brainstem auditory nuclei of the rat. J. Comp. Neurol., 260, 157-174.
50. Obata, K., Oide, M. & Tanaka, H. (1978) Excitatory and inhibitory actions of GABA and glycine on embryonic chick spinal neurons in culture. Brain Res., 144, 179-184.
51. Obrietan, K. & van den Pol, A.N. (1995) GABA neurotransmission in the hypothalamus: Developmental reversal from Ca(2+)elevating to depressing. J. Neurosci., 15, 5065-5077.
52. Oertel, D. (1999) The role of timing in the brain stem auditory nuclei of vertebrates. Annu. Rev. Physiol., 61, 497-519.
53. Owens, D.F., Boyce, L.H., Davis, M.B. & Kriegstein, A.R. (1996) Excitatory GABA responses in embryonic and neonatal cortical slices demonstrated by gramicidin perforated-patch recordings and calcium imaging. J. Neurosci., 16, 6414-6423.
54. Parks, T.N. (1999) Cochlear influences on development of the brainstem auditory system. In Hyson, R.L., Johnson, F. (eds), The Biology of Early Influences. Academic Press, New York, NY, pp. 15-34.
55. Reichling, D.B., Kyrozis, A., Wang, J. & Macdermott, A.B. (1994) Mechanisms of GABA and glycine depolarization-induced calcium transients in rat dorsal horn neurons. J. Physiol. (Lond.), 476, 411-421.
56. Rietzel, H.J. & Friauf, E. (1998) Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J. Comp Neurol., 390, 20-40.
57. Sanes, D.H. & Friauf, E. (2000) Development and influence of inhibition in the lateral superior olivary nucleus. Hear. Res., 147, 46-58.
58. Sanes, D.H., Markowitz, S., Bernstein, J. & Wardlow, J. (1992) The influence of inhibitory afferents on the development of postsynaptic dendritic arbors. J. Comp. Neurol., 321, 637-644.
59. Sanes, D.H. & Siverls, V. (1991) Development and specificity of inhibitory terminal arborizations in the central nervous system. J. Neurobiol., 8, 837-854.
60. Sanes, D.H. & Takacs, C. (1993) Activity-dependent refinement of inhibitory connections. Eur. J. Neurosci., 5, 570-574.
61. i in auditory neurones of developing rats. Neuroreport, 5, 2321-2324.
62. Schwartz, I.R. (1992) The superior olivary complex and lateral lemniscal nuclei. In Webster, B., Popper, A.N., Fay, R.R. (eds), The Mammalian Auditory Pathways: Neuroanatomy. Springer-Verlag, New York, NY, pp. 117-167.
63. A receptors. Science, 269, 977-981.
64. 2+ transients in embryonic rat dorsal horn neurons in culture. Eur. J. Neurosci., 6, 1275-1280.
65. Warr, W.B. & Beck, J.E. (1996) Multiple projections from the ventral nucleus of the trapezoid body in the rat. Hear. Res., 93, 83-101.
66. Wu, S.H. & Kelly, J.B. (1991) Physiological properties of neurons in the mouse superior olive: Membrane characteristics and postsynaptic responses studied in vitro. J. Neurophysiol., 65, 230-246.
67. Wu, S.H. & Kelly, J.B. (1992) Synaptic pharmacology of the superior olivary complex studied in mouse brain slice. J. Neurosci., 12, 3084-3097.
68. 2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron, 6, 333-344.