Glutamate receptors underlying excitatory synaptic transmission in the rat's lateral superior olive studied in vitro

Hearing Research

Volumn 122, Issue 1-2, 1998, Pages 47-59

  Wu, Shu Hui ^a   Fu, Xiao Wen ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

Auditory system; Binaural interaction; Ionotropic glutamate receptor; Metabotropic glutamate receptor; Patch clamp recording; Superior olivary complex

Indexed keywords

1 AMINO 1,3 CYCLOPENTANEDICARBOXYLIC ACID; 2 AMINO 4 PHOSPHONOBUTYRIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; ALPHA METHYL 4 CARBOXYPHENYLGLYCINE; BIOCYTIN; GLUTAMATE RECEPTOR; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; IN VITRO STUDY; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SUPERIOR OLIVARY NUCLEUS;

6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; AMINOBUTYRIC ACIDS; ANIMALS; CYCLOLEUCINE; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; NEUROPROTECTIVE AGENTS; OLIVARY NUCLEUS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 0032145697     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0378-5955(98)00085-9     Document Type: Article

References (83)

1. Aoki E., Semba R., Kato K., Kashiwamata S. Purification of specific antibody against aspartate and immunocytochemical localization of aspartergic neurons in the rat brain. Neuroscience. 21:1987;755-765.
2. Barnes-Davies M., Forsythe I.D. Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. J. Physiol. 488:1995;387-406.
3. Baskys A., Malenka R.C. Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J. Physiol. 444:1991;786-801.
4. Boudreau J.C., Tsuchitani C. Binaural interaction in the cat superior olive S segment. J. Neurophysiol. 31:1968;442-454.
5. Boudreau, J.C. and Tsuchitani, C. (1970) Cat superior olive S-segment cell discharge to tonal stimulation. In: Neff, W.D. (Ed.), Contributions to Sensory Physiology, Vol. 4. Academic Press, New York, pp. 143-213.
6. Browner R.H., Webster D.B. Projections of the trapezoid body and the superior olivary complex of the kangaroo rat (Dipodomys merriami). Brain Behav. Evol. 11:1975;322-354.
7. Brunso-Bechtold J.K., Thompson G.C., Masterton R.B. HRP study of the organization of auditory afferents ascending to the central nucleus of the inferior colliculus. J. Comp. Neurol. 197:1981;705-722.
8. Burke J.P., Hablitz J.J. Presynaptic depression of synaptic transmission mediated by activation of metabotropic glutamate receptors in rat neocortex. J. Neurosci. 14:1994;5120-5130.
9. Caird D., Klinke R. Processing of binaural stimuli by cat superior olivary complex neurons. Exp. Brain Res. 52:1983;385-399.
10. Cant N.B., Casseday J.H. Projection from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J. Comp. Neurol. 247:1986;457-476.
11. Cao C.Q., Evans R.H., Headley P.M., Udvarhelyi P.M. a comparison of the effects of selective metabotropic glutamate receptor agonist on synaptically evoked whole cell currents of rat spinal ventral horn neurones in vitro. Br. J. Pharmacol. 115:1995;1469-1474.
12. Caspary D.M., Faingold C.L. Non-N-methyl-D-aspartate receptors may mediate ipsilateral excitation at lateral olivary synapses. Brain Res. 503:1989;83-90.
13. Caspary, D.M. and Finlayson, P.G., 1991. Superior olivary complex: functional neuropharmacology of the principal cell types. In: Altshuler, R.A., Hoffman, D.W., Bobbin, R.P. and Clopton, B. (Eds.), Neurobiology of Hearing, Vol. 2. Raven Press, New York, pp. 141-161.
14. Casseday J.H., Neff W.D. Auditory localization: role of auditory pathways in brainstem of the cat. J. Neurophysiol. 38:1975;842-858.
15. Covey E., Vater M., Casseday J.H. Binaural properties of single units in the superior olivary complex of the mustached bat. J. Neurophysiol. 66:1991;1080-1094.
16. Elverland H.H. Ascending and intrinsic projections of the superior olivary complex in the cat. Exp. Brain Res. 32:1978;117-134.
17. Finlayson P.G., Caspary D.M. Synaptic potentials of chinchilla lateral superior olivary neurons. Hear. Res. 38:1989;221-228.
18. Forsythe I.D., Barnes-Davies M. The binaural auditory pathway: excitatory amino acid receptors mediate dual time course excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body. Proc. R. Soc. B251:1993;151-157.
19. Forsythe I.D., Westbrook G.L. Slow excitatory postsynaptic currents mediated by activation of N-methyl-D-aspartate receptors on cultured mouse central neurones. J. Physiol. 396:1988;515-534.
20. Fu X.W., Brezden J.B., Kelly J.B., Wu S.H. Synaptic excitation in the dorsal nucleus of the lateral lemniscus: whole-cell patch clamp recordings from rat brain slice. Neuroscience. 78:1997;815-827.
21. Fu X.W., Wu S.H., Kelly J.B. Synaptic excitation and inhibition in the lateral superior olive. Soc. Neurosci. Abstr. 22:1996;648.
22. Gereau IV R.W., Conn P.J. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J. Neurosci. 15:1995;6879-6889.
23. Glaum S.R., Miller R.J. Metabotropic glutamate receptors mediate excitatory transmission in the nucleus of the solitary tract. J. Neurosci. 12:1992;2251-2258.
24. Glendenning K.K., Baker B.N., Hutson K.A., Masterton R.B. Acoustic chiasm. V: Inhibition and excitation in the lateral and contralateral projections of LSO. J. Comp. Neurol. 319:1992;100-122.
25. Glendenning K.K., Hutson K.A., Nudo R.J., Masterton R.B. Acoustic chiasm. II: Anatomical basis of binaurality in lateral superior olive of cat. J. Comp. Neurol. 232:1985;261-285.
26. Glendenning K.K., Masterton R.B., Baker B.N., Wenthold R.L. Acoustic chiasm. III: Nature, distribution, and sources of afferents to the lateral superior olive in the cat. J. Comp. Neurol. 310:1991;377-400.
27. Goldberg J.M., Brown P.B. Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J. Neurophysiol. 31:1968;639-656.
28. Goldberg J.M., Brown P.B. Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol. 32:1969;613-636.
29. Guinan J.J. Jr., Guinan S.S., Norris B.E. Single auditory units in the superior olivary complex. I. Responses to sounds and classifications based on physiological properties. Int. J. Neurosci. 4:1972;101-120.
30. Guinan J.J. Jr., Guinan S.S., Norris B.E. Single auditory units in the superior olivary complex. II. Localizations of unit categories and tonotopic organization. Int. J. Neurosci. 4:1972;147-166.
31. Hamill O.P., Marty A., Nether E., Sakmann B., Sigworth F.J. Improved patch-clamp techniques for high resolution current from cells and cell-free membrane patches. Pflügers Arch. 391:1981;85-100.
32. Harrison, J.M. and Feldman, M.L., 1970. Anatomical aspects of the cochlear nucleus and superior olivary complex. In: Neff, W.D. (Ed.), Contributions to Sensory Physiology, Vol. 4. Academic Press, New York, pp. 95-142.
33. Harrison J.M., Irving R. Ascending connections of the anterior ventral cochlear nucleus in the rat. J. Comp. Neurol. 126:1966;51-64.
34. Harrison J.M., Warr W.B. The cochlear nucleus and ascending pathways of the medulla. J. Comp. Neurol. 11:1962;341-380.
35. Helfert R.H., Schwartz I.R. Morphological evidence for the existence of multiple neuronal classes in the cat lateral superior olivary nucleus. J. Comp. Neurol. 244:1986;533-549.
36. Helfert R.H., Schwartz I.R. Morphological evidence for the presence of five cell types in the gerbil lateral superior olivary nucleus. Am. J. Anat. 179:1987;55-69.
37. Henkel C.K., Brunso-Bechtold J.K. Dendritic morphology and development in the ferret lateral superior olivary nucleus. J. Comp. Neurol. 313:1991;259-272.
38. Hestrin S., Nicoll R.A., Perkel D.L., Sah P. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J. Physiol. 422:1990;203-225.
39. Ishida M., Saitoh T., Shimamoto K., Ohfune Y., Shinozaki H. A novel metabotropic glutamate receptor agonist: Marked depression of monosynaptic excitation in the newborn rat isolated spinal cord. Br. J. Pharmacol. 109:1993;1169-1177.
40. Issacson J.S., Walmsley B. Receptors underlying excitatory synaptic transmission in slices of the rat anteroventral cochlear nucleus. J. Neurophysiol. 73:1995;964-973.
41. Jenkins W.M., Masterton R.B. Sound localization: effects of unilateral lesions in central auditory system. J. Neurophysiol. 47:1982;987-1016.
42. Jonas P., Sakmann B. Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells in rat hippocampal slices. J. Physiol. 455:1992;143-171.
43. Joris P.X., Yin T.C.T. Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences. J. Neurophysiol. 73:1995;1043-1062.
44. Kandler K., Friauf E. Development of glycinergic and glutamate synaptic transmission in the auditory brainstem of perinatal rats. J. Neurosci. 15:1995;6890-6904.
45. Kavanagh G.L., Kelly J.B. Midline and lateral field sound localization in the ferret (Mustela Putorius): contribution of the superior olivary complex. J. Neurophysiol. 67:1992;1643-1658.
46. Kiss K.M. Types of neurons and synaptic relations in the lateral superior olive of the cat: normal structure and experimental observations. Acta Morphol. Hung. 38:1990;207-215.
47. Kotak V.C., Sanes D.H. Synaptically evoked prolonged depolarizations in developing auditory systems. J. Neurophysiol. 74:1995;1611-1620.
48. Kotak V.C., Sanes D.H. Developmental influence of glycinergic transmission: regulation of NMDA receptor-mediated EPSPs. J. Neurosci. 16:1996;1836-1843.
49. Kotak V.C., Sanes D.H. Deafferentation weakens excitatory synapses in the developing central auditory system. Eur. J. Neurosci. 9:1997;2340-2347.
50. Kudo M., Nakamura Y., Tokuno H., Kitao Y. Auditory brain stem in the mole (Mogera): nuclear configurations and the projections to the inferior colliculus. J. Comp. Neurol. 298:1990;400-412.
51. Lachica E.A., Rübsamen R., Zirpel L., Rubel E.W. Glutamatergic inhibition of voltage-operated calcium channels in the avian cochlear nucleus. J. Neurosci. 15:1995;1724-1734.
52. Madl J.E., Larson A.A., Beitz A.J. Monoclonal antibody specific for carbodiimide-fixed glutamate: immunocytochemical localization in the rat CNS. J. Histochem. Cytochem. 34:1986;317-326.
53. Manis P.B., Molitor S.C. N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus. J. Neurophysiol. 76:1996;1639-1656.
54. Manzoni O., Bockaert J. Metabotropic glutamate receptors inhibiting excitatory synapses in the CA1 area of rat hippocampus. Eur. J. Neurosci. 7:1995;2518-2523.
55. Manzoni O.J., Castillo P.E., Nicoll R.A. Pharmacology of metabotropic glutamate receptors at the mossy fiber synapses of the guinea pig hippocampus. Neuropharmacology. 34:1995;965-971.
56. Masterton R.B., Jane J.A., Diamond I.T. Role of brainstem auditory structures in sound localization. I. Trapezoid body, superior olive, and lateral lemniscus. J. Neurophysiol. 30:1967;341-459.
57. Mayer L.M., Westbrook G.L. Permeation and block of N-methyl-D-aspartic acid receptor channels by divalent cations in mouse cultured central neurons. J. Physiol. (Lond.). 394:1987;501-527.
58. Molitor S.C., Manis P.B. Evidence for functional metabotropic glutamate receptors in the dorsal cochlear nucleus. J. Neurophysiol. 77:1997;1889-1905.
59. Moore D.R. Auditory brainstem of the ferret: sources of projections to the inferior colliculus. J. Comp. Neurol. 269:1988;342-354.
60. Moore C.N., Moore C.N., Casseday J.H., Neff W.D. Sound localization: role of the commissural pathways of the auditory system of the cat. Brain Res. 82:1974;13-26.
61. Nakanishi S. Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron. 13:1994;1031-1037.
62. Ollo C., Schwartz I.R. The superior olivary complex in C57BL/6 mice. Am. J. Anat. 155:1979;349-374.
63. Sanes D.H. An in vitro analysis of sound localization mechanisms in the gerbil superior olive. J. Neurosci. 10:1990;3494-3506.
64. Sato K., Kuriyama H., Bonneau J.M., Altschuler R.A. Expression of NMDA-receptor mRNA in the rat cochlear nucleus and superior olivary complex. Assoc. Res. Otolaryngol. Abstr. 18:1995;31.
65. Schofield B.R., Cant N.B. Organization of the superior olivary complex in the guinea pig. I. Cytoarchitecture, cytochrome oxidase histochemistry, and dendritic morphology. J. Comp. Neurol. 314:1991;645-670.
66. Stotler W.A. An experimental study of the cells and connections of the superior olivary complex of the cat. J. Comp. Neurol. 98:1953;401-431.
67. Strominger N.L., Strominger A.I. Ascending brain stem projections of the anteroventral cochlear nucleus in the rhesus monkeys. J. Comp. Neurol. 143:1971;217-242.
68. 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.
69. Takahashi T., Momiyama A., Cull-Candy S.G. Presynaptic receptors for the glutamate analogue APB reduce transmitter release from neonatal rat spinal cord neurones in thin slices. J. Physiol. 446:1992;549P.
70. 2+-dependent non-NMDA receptor-mediated synaptic currents in ischemic CA1 hippocampal neurons. J. Neurophysiol. 71:1994;1190-1196.
71. Tsuchitani C. Functional organization of lateral cell groups of cat superior olivary complex. J. Neurophysiol. 40:1977;296-318.
72. Tsuchitani C., Boudreau J.C. Stimulus level of dichotically presented tones and cat superior olive S-segment cell discharge. J. Acoust. Soc. Am. 46:1969;978-988.
73. Warr W.B. Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat. Exp. Neurol. 14:1966;453-474.
74. Warr W.B. Fiber degeneration following lesions in the multipolar and globular cells areas in the ventral cochlear nucleus of the cat. Brain Res. 40:1972;247-270.
75. Warr, W.B., 1982. Parallel ascending pathways from the cochlear nucleus: neuroanatomical evidence of functional specialization. In: Neff, W.D., (Ed.), Contributions to Sensory Physiology, Vol. 7. Academic Press, New York, pp. 1-38.
76. Wu S.H., Kelly J.B. Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro. J. Neurophysiol. 65:1991;230-246.
77. Wu S.H., Kelly J.B. Binaural interaction in the lateral superior olive: time difference sensitivity studied in mouse brain slice. J. Neurophysiol. 68:1992;1151-1159.
78. Wu S.H., Kelly J.B. NMDA, non-NMDA and glycine receptors mediate binaural interaction in the superior olive: physiological evidence from mouse brain slice. Neurosci. Lett. 134:1992;257-260.
79. Wu S.H., Kelly J.B. Synaptic pharmacology of the superior olivary complex studied in mouse brain slice. J. Neurosci. 12:1992;3084-3097.
80. Zhang S., Trussell L. Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. J. Physiol. 480:1994;123-136.
81. Zhou N., 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. 67:1992;145-152.
82. 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.
83. Zirpel L., Rubel E. Eighth nerve activity regulates intracellular calcium concentration of avian cochlear neurons via a metabotropic glutamate receptor. J. Neurophysiol. 76:1996;4127-4139.