Cellular approach to auditory signal transmission

Japanese Journal of Physiology

Volumn 46, Issue 4, 1996, Pages 289-310

  Koyano, Konomi ^a   Ohmori, Harunori ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Auditory system; Cochlea; Cochlear nucleus; Hair cell; Superior olivary complex

Indexed keywords

GLUTAMIC ACID; ION CHANNEL; NEUROTRANSMITTER;

AUDITORY SYSTEM; HAIR CELL; ION CURRENT; NEUROTRANSMITTER RELEASE; NONHUMAN; POSTSYNAPTIC POTENTIAL; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 0029858719     PISSN: 0021521X     EISSN: None     Source Type: Journal    
DOI: 10.2170/jjphysiol.46.289     Document Type: Review

References (195)

1. Spoendlin H: Efferent innervation of the cochlea In: Comparative Physiology of Sensory System, ed. Bolis L, Keynes RD, and Maddrell SHP, Cambridge University Press, Cambridge, pp 163-188, 1984
2. Knudsen EI: Space coding in the vertebrate auditory system. In: Bioacoustics A Comparative Approach, ed Lewis B, Academic Press, New York, pp 311-344, 1983
3. Goldberg JM and Brown PB: Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J Neurophysiol 32: 613-636, 1969
4. Moiseff A and Konishi M: Binaural characteristics of units in the owl's brainstem auditory pathway precursors of restricted spacial receptive fields. J Neurosci 3: 2553-2562, 1983
5. Hudspeth AJ: Mechanoelectrical transduction by hair cells in the acousticolateralis sensory system. Annu Rev Neurosci 6: 187-215, 1983
6. Hudspeth AJ. How the ear's works work Nature 341: 397-404, 1989
7. Hudspeth AJ and Gillespie PG: Pulling strings to tune transduction: adaptation by hair cells. Neuron 12: 1-9, 1994
8. Ashmore JF: The electrophysiology of hair cells. Annu Rev Physiol 53: 465-476, 1991
9. Ohmori H: Ion channels for the mechano-etectrical transduction and efferent synapse of the hair cell. Adv Biophys 28: 1-30, 1992
10. Corey DP and Hudspeth AJ: Analysis of the microphonic potential of the bullfrog's sacculus. J Neurosci 3: 945-961, 1983
11. Ohmori H. Mechano-electrical transduction currents in isolated vestibular hair cells of the chick. J Physiol (Lond) 359: 189-217, 1985
12. Ohmori H: Gating properties of the mechano-electrical transduction channel in the dissociated vestibular hair cell of the chick J Physiol (Lond) 387: 589-609, 1987
13. Crawford AC, Evans MG, and Fettiplace R: The actions of calcium on the mochano-electrical transducer current of turtle hair cells. J Physiol (Lond) 434: 369-398, 1991
14. Davis H: A model for transducer action in the cochlea In: Symposia on Quantitative Biology, Cold Spring Harbor Laboratory of Quantitative Biology, New York, Vol 30, pp 181-190, 1965
15. Citron L, Exley D, and Hallpike CS: Formation, circulation and chemical properties of the labyrinthine fluid. Br Med Bull 12: 101-104, 1956
16. Bosher SK and Warren RL: Observations on the electrochemistry of the cochlear endolymph of the rat. Proc R Soc B171: 227-247, 1968
17. Bosher SK and Warren RL: Very low calcium content of cochlear endolymph, an extracellular fluid. Nature 273: 377-378, 1978
18. Sellick PM and Johnstone BM: Production and role of inner ear fluid. Prog Neurobiol 5: 337-362, 1975
19. Rhode W Observations of the vibration of the basilar membrane in squirrel monkeys using the Moesbauer technique. J Acoust Soc Am 49: 1218-1231, 1971
20. Khana SM and Leonard DGB: Basilar membrane tuning in the cat cochlea Science 215: 305-306, 1982
21. Sellick PM, Patuzzi R, and Johnstone BM. Measurement of basilar membrane motion in the guinea pig using the Moesbauer technique. J Acoust Soc Am 72: 131-141, 1982
22. von Bekesy G: Experiments in Hearing, McGraw-Hill, New York, pp 403-534, 1960
23. Lewis RS and Hudspeth AJ: Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature 304: 538-541, 1983
24. Hagiwara S and Byerly L: Calcium channel. Annu Rev Neurosci 4: 69-125, 1981
25. Ohmori H: Studies of ionic currents in the isolated vestibular hair cell of the chick. J Physiol (Lond) 350: 561-581, 1984
26. Art JJ and Fettiplace R. Variation of membrane properties in hair cells isolated from the turtle cochlea. J Physiol (Lond) 385: 207-242, 1987
27. Hudspeth AJ and Lewis RS: Kinetic analysis of voltage- and ion-dependent conductances in saccular hair cells of the bull-frog, Rana catesbeiana. J Physiol (Lond) 400: 237-274, 1988
28. Fuchs PA, Evans MG, and Murrow BW: Calcium currents in hair cells isolated from the cochlea of the chick. J Physiol (Lond) 429: 553-568, 1990
29. Art JJ, Fettiplace R, and Wu Y-C. The effects of low calcium on the voltage-dependent conductances involved in tuning of turtle hair cells J Physiol (Lond) 470: 109-126, 1993
30. Fox AP, Nowycky MC, and Tsien RW: Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones J Physiol (Lond) 394: 149-172, 1987
31. Hagiwara S and Ohmori H: Studies of calcium channels in rat clonal pituitary cells with patch electrode voltage clamp. J Physiol (Lond) 331: 231-252, 1982
32. Fenwick EM, Marty A, and Neher E: Sodium and calcium channels in bovine chromaffin cells. J Physiol (Lond) 331: 599-635, 1982
33. Roberts WM, Jacobs RA, and Hudspeth AJ: Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci 10: 3664-3684, 1990
34. Crawford AC and Fettiplace R: The frequency selectivity of auditory nerve fibres and hair cells in the cochlea of the turtle. J Physiol (Lond) 306: 79-125, 1980
35. Ashmore JF: Frequency tuning m a frog vestibular organ. Nature 304: 536-538, 1983
36. Sugihara I and Furukawa T: Morphological and functional aspects of two different types of hair cells in the goldfish sacculus J Neurophysiol 62: 1330-1343, 1989
37. Fuchs PA and Evans MG: Potassium currents in hair cells isolated from the cochlea of the chick. J Physiol (Lond) 429: 529-551, 1990
38. Sugihara I: Calcium activated potassium channels in goldfish hair cells. J Physiol (Lond) 476: 373-390, 1994
39. Houseley GD and Ashmore JF. Ionic currents of outer hair cells isolated from the guinea-pig cochlea. J Physiol (Lond) 448: 73-98, 1992
40. Kros CJ and Crawford AC: Potassium currents in inner hair cells isolated from the guinea pig cochlea. J Physiol (Lond) 421: 263-291, 1990
41. 2+ chelators Pflügers Arch 430: 365-373, 1995
42. Masetto S, Russo G, and Prigioni I: Differential expression of potassium currents by hair cells in thin slices of frog crista ampullaris. J Neurophysiol 72: 443-455, 1994
43. A) by 'short' hair cells of the chick. Proc R Soc Lond B 242: 189-195, 1990
44. Hagiwara S and Takahashi K: The anomalous rectification and cation selectivity of the membrane of a starfish egg cell. J Membr Biol 18: 61-80, 1974
45. Ohmori H: Inactivation kinetics and steady-state current noise in anomalous rectifier of tunicate egg cell membranes J Physiol (Lond) 281: 77-99, 1978
46. Evans MG and Fuchs PA. Tetrodotoxin-sensitive, voltage-dependent sodium currents in hair cells from the alligator cochlea. Biophys J 52: 649-652, 1987
47. Witt CM, Brownell WE, and Bertrand D. Physiologically silent sodium channels in mammalian outer hair cells J Neurophysiol 72: 1037-1040, 1994
48. Kiang NYS, Watanabe T, Thomas EC, and Clark LF Discharge patterns of single fibers in the cat's auditory nerve. In: Research Monograph 35, MIT Press, Cambridge, MA, 1965
49. Dallos P: Cochlear neurobiology: some key experiments and concepts of the past two decades. In: Auditory Function, ed Edelman GM, Gall WE, and Cowan WM, John Wiley & Sons, New York, Chapter 5, pp 153-188, 1988
50. Eatock RA, Saeki M, and Hutzler MJ: Electrical resonance of isolated hair cells does not account for acoustic tuning in the free-standing region of the alligator lizard's cochlea. J Neurosci 13: 1767-1783, 1993
51. Hudspeth AJ and Corey DP: Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc Natl Acad Sci USA 74: 2407-2411, 1977
52. Fuchs PA, Nagai T, and Evans MG. Electrical tuning in hair cells isolated from the chick cochlea J Neurosci 8: 2460-2467, 1988
53. Kataoka Y and Ohmori H: Activation of glutamate receptors in response to membrane depolarization of hair cells isolated from chick cochlea. J Physiol (Lond) 477: 403-414, 1994
54. + current in rat hippocampal neurones. J Physiol (Lond) 475: 229-239, 1994
55. Adler EM, Augstine GJ, Duffy SN, and Charlton MP: Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci 11: 1496-1507, 1991
56. Zucker RS: Calcium and transmitter release. J Physiol (Paris) 87: 25-36, 1993
57. Parsons TD, Lentzi D, Almers W, and Roberts W. Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 13: 875-883, 1994
58. + channels at fluorescently labeled presynaptic active zones of hair cells. Proc Natl Acad Sci USA 91: 7578-7582, 1994
59. Furukawa T and Ishii Y: Neurophysiological studies on hearing in goldfish. J Neurophysiol 30: 1377-1403, 1967
60. Furukawa T and Matsuura S: Adaptive rundown of excitatory post-synaptic potentials at synapses between hair cells and eighth nerve fibers in the goldfish. J Physiol (Lond) 276: 193-209, 1978
61. Crawford AC, Evans MG, and Fettiplace R: Activation and adaptation of transducer currents in turtle hair cells. J Physiol (Lond) 419: 405-434, 1989
62. Kimitsuki T and Ohmori H: The effect of caged calcium release on the adaptation of the transduction current in the chick hair cells. J Physiol (Lond) 458: 27-40, 1992
63. Kuno M. Adaptive changes in firing rates in goldfish auditory fibers as related to changes in mean amplitude of excitatory postsynaptic potentials. J Neurophysiol 50: 573-581, 1983
64. Furukawa T, Hayashida Y, and Matsuura S: Quantal analysis of the size of excitatory postsynaptic potentials at synapses between hair cells and afferent fibers in goldfish. J Physiol (Lond) 276: 211-226, 1978
65. Furukawa T, Kuno M, and Matsuura S: Quantal analysis of a decremental response at hair cell-afferent fiber synapses in the goldfish sacculus. J Physiol (Lond) 322: 181-195, 1982
66. Bobbin RP: Glutamate and aspartate mimic the afferent transmitter in the cochlea. Exp Brain Res 34: 389-393, 1979
67. Bobbin RP and Thompson MH: Effects of putative transmitters on afferent cochlea transmission. Ann Otol Rhinol Laryngol 87: 185-190, 1978
68. Comis SD and Leng G: Action of putative neurotransmitters in the guinea-pig cochlea. Exp Brain Res 36: 119-128, 1979
69. Guth P, Norris CH, and Barron SE: Three tests of the hypothesis that glutamate is the sensory hair cell transmitter in the frog semicircular canal. Hear Res 33: 223-228, 1988
70. Flock A and Lam DMK: Neurotransmitter synthesis in inner ear and lateral line sense organs. Nature 249: 142-144, 1974
71. Sewell WF, Norris CH, Tachibana M, and Guth PS: Detection of an auditory nerve-activating sutastance(s). Science 202: 910-912, 1978
72. Sewell WF and Mroz EA: Neuroactive substances in inner ear extracts J Neurosci 7: 2465-2475, 1987
73. Eybalin M. Neurotransmitters and neuromodulators of the mammalian cochlea Physiol Rev 73: 309-373, 1993
74. Niedzielski AS and Wenthold RJ. Expression of AMPA, kainate and NMDA receptor subunits in cochlear and vestibular ganglia. J Neurosci 15: 2338-2353, 1995
75. Usami S, Matsubara A, Fujita S, Shinkawa H, and Hayashi M: NMDA (NMDAR1) and AMPA (GluR2/3) receptor subunits are expressed in the inner ear. Neuroreport 6: 1161-1164, 1995
76. Puel JL, Pujol R, Tribillac F, Ladrech S, and Eybalin M: Excitatory amino acid antagonists protect cochlear auditory neurons from excitotoxicity. J Comp Neurol 341: 241-256, 1994
77. Yamaguchi K and Ohmori H: Voltage-gated and chemically gated ionic channels in the cultured cochlear ganglion neurone of the chick. J Physiol (Lond) 420: 185-206, 1990
78. Nakagawa T, Komune S, Uemura T, and Akaike N: Excitatory amino acid response in isolated spiral ganglion cells of guinea pig cochlea. J Neurophysiol 65 715-723, 1991
79. Horn R and Marty A: Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92: 145-159, 1988
80. Mayer ML and Westbrook GL: The physiology of excitatory amino acids in the vertebrate central nervous system. Prog Neurobiol 28: 197-276, 1987
81. Kataoka Y and Ohmori H: Of known neurotransmitters, glutamate is the most likely to be released from chick cochlear hair cells. J Neurophysiol. 1996 (in press)
82. Atwell D, Barbour B, and Szatkowski M: Nonvesicular release of neurotransmitter. Neuron 11: 401-407, 1993
83. Kanai Y, Smith CP, and Hediger MA: The elusive transporters with a high affinity for glutamate. Trends Neurosci 16: 365-370, 1993
84. 3H]L-glutamine uptake in the guinea-pig cochlea Neuroscience 9: 863-871, 1983
85. Ryanv AF and Schwartz IR. Preferential glutamine uptake by cochlear hair cells: implications for the afferent cochlear transmitter. Brain Res 290: 376-379, 1984
86. Annoni J-M, Cochran SL, and Precht W. Pharmacology of the vestibular hair cell-afferent fiber synapse in the frog. J Neurosci 4 2106-2116, 1984
87. Rossi ML, Martini M, Pelucchi B, and Fesce R: Quantal nature of synaptic transmission at the cytoneural junction in the frog labyrinth. J Physiol (Lond) 478: 17-35, 1994
88. Yamashita M and Ohmori H: Synaptic responses to mechanical stimulation in calyceal and button type vestibular afferents studied in an isolated preparation of semicircular canal ampullae of chicken. Exp Brain Res 80: 475-488, 1990
89. Raman IM and Trussell LO: The kinetics of the response to glutamate and kinate in neurons of the avian cochlear nucleus. Neuron 9: 173-186, 1992
90. Sommer B, Keinaenen K, Verdoorn T, Wisden W, Burnashev N, Herb A, Koehler M, Takagi T, Sakmann B, and Seeburg PH. Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249: 1580-1585, 1990
91. Ascher P and Nowak L: The role of divalent cations in the N-methyl-D-aspartate responses of mouse central neurones in culture. J Physiol (Lond) 399: 247-266, 1988
92. 2+ concentration in chick cochlear hair cells. J Physiol (Lond) 420: 127-148, 1990
93. + channels. J Physiol (Lond) 442: 669-690, 1991
94. Fuchs PA and Murrow BW Cholinergic inhibition of short (outer) hair cells of the chick's cochlea J Neurosci 12: 800-809, 1992
95. Kakehata S, Nakagawa T, Takasaka T, and Akaike N. Cellular mechanism of ACh-induced response in dissociated outer hair cells of guinea-pig cochlea J Physiol (Lond) 463: 227-244, 1993
96. 2+ concentration and hyperpolarizes the guinea-pig outer hair cell. Hear Res 67: 179-188, 1993
97. Evans MG: Acetylcholine activates two currents in guinea-pig outer hair cells. J Physiol (Lond) 491: 563-578, 1996
98. Yoshida N, Sigemoto T, Sugai T, and Ohmori H. The role of inositol trisphosphate on ACh-induced outward currents in bullfrog saccular hair cells. Brain Res 644: 90-100, 1994
99. Ohtani M, Devau G, Lehouelleur J, and Sans A Cholinergic agonists increase intracellular calcium concentration in frog vestibular hair cells Hear Res 80 167-173, 1994
100. Elgoyhen AB, Johnson DS, Boulter J, Vetter DE, and Heinemann S: α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79: 705-715, 1994
101. Furukawa T: Effects of efferent stimulation on the saccute of goldfish. J Physiol (Lond) 315: 203-215, 1981
102. Art JJ, Fettiplace R, and Fuchs PA: Synaptic hyperpolarization and inhibition of turtle cochlear hair cells. J Physiol (Lond) 356: 525-550, 1984
103. Goldberg JM and Fernandez C: Efferent vestibular system in the squirrel monkey, anatomical location and influence on afferent activity. J Neurophysiol 43: 986-1025, 1980
104. Highstein SM and Baker R: Action of the efferent vestibular system on primary afferent in the toadfish, Opsanus tau. J Neurophysiol 54: 370-384, 1985
105. Norris CH, Houseley GD, Williams WH, Guth SL, and Guth PS: The acetylcholine receptors of the semicircular canal in the frog (Rana pipiens). Hear Res 32: 197-206, 1988
106. + current by cholinergic agonists in cultured cochlear ganglion neurones. J Physiol (Lond) 464: 213-228, 1993
107. Brownell WE, Bader CR, Bertrand D, and de Ribaupierre Y: Evoked mechanical responses of isolated cochlear outer hair cells Science 227: 194-196, 1984
108. Ashmore JF: A fast motile response in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. J Physiol (Lond) 388: 323-347, 1987
109. Santos-Sacchi J: Asymmetry in voltage-dependent movements of isolated outer hair cells from the organ of corti. J Neurosci 9 2954-2965, 1989
110. Brundin L, Flock A, and Canlon B: Sound-induced motility of isolated cochlear outer hair cells is frequency-specific. Nature 342: 814-816, 1989
111. Dallos P. The active cochlea. J Neurosci 12: 4575-4585, 1992
112. Ruggero MA and Rich NC: Furosemide alters organ of corti mechanics: evidence for feedback of outer hair cells upon the basilar membrane. J Neurosci 11: 1057-1067, 1991
113. Sullivan EW and Konishi M: Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl. J Neurosci 4: 1787-1799, 1984
114. Takahashi T, Moiseff A, and Konishi M: Time and intensity cues are processed independently in the auditory system of the owl J Neurosci 4: 1781-1786, 1984
115. Konishi M: Listening with two ears. Sci Am 268: 66-73, 1993
116. Carr CE and Konishi M: A circuit for detection of interaural time difference in the brainstem of the barn owl. J Neurosci 10: 3227-3246, 1990
117. Overholt EM, Rubel EW, and Hyson RL: A circuit for coding interaural time differences in the chick brain stern. J Neurosci 12: 1698-1780, 1992
118. Jeffress LA: A place theory of sound localization. J Comp Physiol Psychol 41: 35-39, 1948
119. Carr CE: Processing of temporal information in the brain. Annu Rev Neurosci 16: 223-243, 1993
120. Knudsen EI and Knudsen PF: Space-mapped auditory projections from the inferior colliculus to the optic tectum in the barn owl (Tyto alba). J Comp Neurol 218: 187-196, 1983
121. Knudsen EI and Knudsen PF: Vision calibrates sound localization in developing barn owl. J Neurosci 10: 222-232, 1989
122. Hotta T: Unit responses from the nucleus angularis in the pigeon's medulla. Comp Biochem Physiol 40A 415-424, 1971
123. Wachol ME and Dallos P: Neuronal coding in the chick cochlear nucleus. J Comp Physiol A 166: 721-734, 1989
124. Smith PH, Joris PX, and Yin TCT. Projection of physiologically characterized spherical bushy cell axons from the cochlear nucleus of the cat: evidence for delay lines to the medial superior olive. J Comp Neurol 331: 245-260, 1993
125. Spitzer MW and Semple MN: Neurons sensitive to interaural phase disparity in gerbil superior olive: diverse monoaural and temporal respons properties. J Neurophysiol 73: 1668-1690, 1995
126. Oertel D: Synaptic responses and electrical properties of the cell in brain slices of the mouse anteroventral cochlear nucleus. J Neurosci 3: 2043-2053, 1983
127. Wu SH and Oertel D: Intracellular injection with horse radish peroxidase of physiologically characterized stellate and bushy cell in slices of mouse anteroventral cochlear nucleus. J Neurosci 4: 1577-1588, 1984
128. Ryes AD, Rubel EW, and Spain WJ Membrane properties underlying the firing of neurons in the avian cochlear nucleus. J Neurosci 14: 5352-5364, 1994
129. Koyano K, Funabiki K, and Ohmori H: Voltage-gated ionic currents and their roles in timing coding in auditory neurons of N. magnocellularis of the chick. Neurosci Res 26: 29-45, 1996
130. Koyano K and Funabiki K: Membrane properties of the neuron of the chick auditory nucleus: Nucleus magnocellularis. Neurosci Res Suppl 18: s190, 1993
131. Koyano K and Funabiki K: Membrane properties of the neuron in avian cochlear nucleus: N. magnocellularis. Jpn J Physiol 44 (Suppl): S183, 1994
132. Zhang S and Trussell LO: A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72: 705-718, 1994
133. Manis PB and Marx SO: Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 11: 2865-2880, 1991
134. + current in hippocampal neurons. Nature 336: 379-381, 1988
135. Isaacson JS and Walmsley B: Receptors underlying excitatory synaptic transmission in slice of the rat anteroventral cochlear nucleus. J Neurophysiol 73: 964-973, 1995
136. Perney TM, Marshall J, Martin KA, Hockfield S, and Kaczmarek LK. Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. J Neurophysiol 164: 435-448, 1992
137. Grissmer S, Nguyen AN, Aiyer J, Hanson DC, Mather RJ, Gutman GA, Karmilowicz MJ, Auperin DD, and Chandy KG:. Pharmacological characterization of five cloned voltage-gated K channels, types Kv1 1, 1 2, 1.3, 1.5 and 3.1, stably expressed in mammalian cell lines. Mol Pharmacol 45: 1227-1234, 1994
138. Rubel EW and Parks TN: Organization and development of brain stem auditory nuclei of the chicken: tonotopic organization of N magnocellularis and N laminaris J Comp Neurol 164: 411-434, 1975
139. Parks TN: Morphology of axosomatic endings in an avian cochlear nucleus: nucleus magnocellularis of the chicken. J Comp Neurol 203: 425-440, 1981
140. Jhaveri S and Morest DK: Sequential alterations of neuronal archtecture in nucleus magnocellularis of the developing chicken, an electron microscope study. Neuroscience 7: 855-870, 1982
141. Sivaramakrishnan S and Laurent G. Pharmacological characterization of presynaptic calcium currents underlying glutamatergic transmission in the avian auditory brainstem. J Neurosci 15: 6576-6583, 1995
142. Raman IM, Zhang S, and Trussell LO: Pathway-specific variants of AMPA receptors and their contribution to neuronal signaling. J Neurosci 14: 4998-5010, 1994
143. Trussell LO, Zhang S, and Raman IM: Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10: 1185-1196, 1993
144. Trussell LO and Fischbach GD: Glutamate desensitization and its role in synaptic transmission. Neuron 3: 209-218, 1989
145. Ryugo DK and Sento S: Synaptic connections of the auditory nerve in cats, relationship between end bulb of Held and spherical bushy cells. J Comp Neurol 305: 35-48, 1991
146. Zhang S and Trussell LO: Voltage clamp analysis of excitatory synaptic transmission in the avian nucleus magnocellularis. J Physiol (Lond) 480: 132-136, 1994
147. Lachica EA, Rubsamen R, Zirpel L, and Rubel EW: Glutamatergic inhibition of voltage-gated calcium channels in the avian cochlear nucleus. J Neurosci 15: 1724-1734, 1995
148. Hyson RL, Ryes AD, and Rubel EW: A depolarizing inhibitory response to GABA in brainstem auditory neurons of the chick. Brain Res 677: 117-126, 1995
149. Parks TN and Rubel EW: Organization of projections from N. magnocellularis to N. laminaris. J Comp Neurol 164: 435-448, 1975
150. Smith DJ and Rubel EW: Organization and development of brain stem auditory nuclei of the chicken: dendritic gradient in nucleus laminaris J Comp Neurol 186: 213-239, 1979
151. Funabiki K, Koyano K, and Ohmori H: Postsynaptic responses of the nucleus laminaris of the chick. Soc Neurosci Abstr 21 (1): 128, 1995
152. Lachica EA, Rubsamen R, and Rubel EW: GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus J Comp Neurol 348: 403-418, 1994
153. Funabiki K, Koyano K, and Ohmori H: GABAergic inpus to the N laminaris of the chick: an increment of accuracy for sound localization. Abstract of the XIXth Midwinter Research Meeting of the Association for Research in Otolaryngology, p 116 (#462), 1996
154. Fujita I and Konishi M: The role of GABAergic inhibition in processing of interaural time difference in the owls, auditory system. J Neurosci 11: 722-739, 1991
155. Reyes AD, Rubel EW, and Spain WJ: In vitro analysis of optimal stimuli for phase-locking and time-delayed modulation of firing in avian N. laminaris neurons. J Neurosci 16: 933-1007, 1996
156. Lippe W and Rubel EW: Ontogeny of tonotopic organization of brain stem auditory nuclei in the chicken: implications for development of the place principle. J Comp Neurol 237: 273-289, 1985
157. Boudreau JC and Tsuchutani C: Binaural interaction in the cat superior olive s-segment. J Neurophysiol 31: 442-454, 1968
158. Moushegian G, Rupert AL, and Gidda JS. Functional characteristics of superior olivary neurons to binaural stimuli. J Neurophysiol 38: 1037-1049, 1975
159. Crow G, Rupert AL, and Moushegian G: Phase locking in monoaural and binaural medullary neurons: implications for binaural phenomena. J Acoust Soc Am 64: 493-501, 1978
160. Yin TCT and Chan JCK: Interaural time sensitivity in medial superior olive of cat. J Neurophysiol 64: 465-488, 1990
161. Kiss A and Majorossy K: Neuron morphology and synaptic architecture of the medial superior olive nucleus. Exp Brain Res 51: 315-327, 1983
162. Spangler KM, Warr WB, and Henkel CK: The projection of principal cell of the medial nucleus of the trapezoid body in the cat J Comp Neurol 238: 249-262, 1985
163. Kuwabara N and Zook JM. Projections in the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. J Comp Neurol 324: 522-538, 1992
164. Grothe B, Vater M, Casseday JH, and Covey E. Monoaural interaction of excitation and inhibition in the medial superior olive of the mustached bat: an adaptation for biosonar. Proc Natl Acad Sci USA 89: 5108-5112, 1992
165. Grothe B and Saines DH: Bilateral inhibition by glycinergic afferents in the medial superior olive. J Neurophysiol 31: 613-636, 1993
166. Grothe B and Sanes DH: Synaptic inhibition influences the temporal coding properties of medial superior olivary neurons. An in vitro study J Neurosci 14: 1701-1709, 1994
167. Smith PH Structual and functional differences distinguish principal from nonprincipal cells in the guinea pig MSO slice. J Neurophysiol 73: 1653-1667, 1995
168. Morest DK: The cellular basis for signal processing in the mammalian cochlear nuclei In The Mammaliam Cochlear Nuclei: Organization and Function, ed. Merchan MA, Juiz JM, Godfrey DA, and Mugnaini E, Plenum, New York and London, pp 1-18, 1991
169. Forsythe ID and Barnes-Davis M: The binauarl 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 Lond B 251: 151-157, 1993
170. Brownell WE: Organization of cat trapezoid body and discharge characteristics of its fibers. Brain Res 94: 413-433, 1975
171. Tsuchitani C and Johnson DH: Binaural cues and signal processing in the superior olivary complex. In: Neurobiology of Hearing: The Current Auditory System, ed. Altschuler RA, Bobbin RP, Clopton BM, and Hoffman DW, Raven, New York, pp 163-193, 1991
172. Wu SH and Kelly JB: Physiological properties of neurons in the mouse superior olive: membrane characteristics and postsynaptic responses studied in vitro. J Neurophysiol 65: 230-246, 1991
173. Banks MI and Smith PH: Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J Neurosci 12: 2819-2837, 1992
174. Forsythe ID and Barnes-Davis M: The binaural auditory pathway: membrane currents limiting multiple action potential generation in the rat medial nucleus of the trapezoid body. Proc R Soc Lond B 251: 142-150, 1993
175. Forsythe ID and Barnes-Davis M: The binaural auditory pathway excitatory amino acid receptors mediate dual timecourse excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body. Proc R Soc Lond B 251: 151-157, 1993
176. Forsythe ID: Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol (Lond) 479: 381-387, 1994
177. + conductances with complementary functions in postsynaptic integration at a central auditory synapse J Neurosci 15: 8011-8022, 1995
178. Brost JJG, Helmchen F, and Sakmann B: Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J Physiol (Lond) 489: 825-840, 1995
179. h) in neurons of the medial nucleus of the trapezoid body: voltage-clamp analysis and enhancement by norepinephrine and cAMP suggest a modulatory mechanism in the auditory brain stem. J Neurophysiol 70: 1420-1432, 1993
180. Yanagihara K and Irisawa H: Inward current activated during hyperpolarization in the rabbit sinoatrial node cell. Pflugers Arch 385: 11-19, 1980
181. f) in cells isolated from the rabbit sino-atrial node. J Physiol (Lond) 377: 61-88, 1986
182. Halliwell JV and Adams PR. Voltage-clamp analysis of muscarinic excitation in hippocampal neurons Brain Res 250: 71-92, 1982
183. Rusznak Z, Forsythe ID, and Stanfield PR: Membrane properties of bushy neurones from the rat anteroventral cochlear nucleus (aVCN) studied using a brain slice preparation. Abstacts of the 2nd Joint Meeting of the Physiological Societies of Japan, UK and Eire, p 27, 1995
184. Kossel M and Vater M: Noradrenaline enhances temporal auditory contrast and neuronal timing precision in the cochlear nucleus of the mustached bat. J Neurosci 9: 4169-4178, 1989
185. Tsuchitani C and Boudreau JC: Stimulus level of dichotically presented tones and cat superior olive s-segment cell discharge. J Acoust Soc Am 46: 978-988, 1969
186. Boudreau JC and Tsuchitani C. Cat superior olive s-segment cell discharge to tonal stimulation. In: Contributions to Sensory Physiology, ed Neff WD, Academic Press, New York, pp 144-213, 1970
187. Tsuchitani C: Discharge patterns of cat lateral superior olivary units to ipsilateral tone-burst stimuli. J Neurophysiol 47: 479-500, 1982
188. Wu SH and Kelly JB: Binaual interaction in the lateral superior olive: time difference sensitivity studied in mouse brain slice. J Neurophysiol 68: 1158-1159, 1992
189. Wu SH and Kelly JB: NMDA, non-NMDA and glycine receptors mediate binaural interaction in the lateral superior olive: physiological evidence from mouse brain slice. Neurosci Lett 134: 257-260, 1992
190. Finlayson PG and Caspary DM: Low-frequency neurons in the lateral superior olive exibit phase-sensitive binaural inhibition. J Neurophysiol 65: 598-605, 1991
191. Joris PX and Yin TCT: Envelope coding in the lateral superior olive. I. Sensitivity to interaural time differences J Neurophysiol 73:1043-1062, 1995
192. Llinas R, Steinberg IZ, and Walton K: Presynaptic calcium currents in squid giant synapse. Biophys J 33: 289-322, 1981
193. Augustine GJ, Charlton MP, and Smith SJ: Calcium action in synaptic transmitter release. Annu Rev Neurosci 10: 633-693, 1987
194. Yawo H and Momiyama A: Re-evaluation of calcium currents in pre- and postsynaptic neurones of the chick ciliary ganglion. J Physiol (Lond) 460: 153-172, 1993
195. Yawo H and Chuhma N: ω-Conotoxin-sensitive and -resistant transmitter release from the chick ciliary presynaptic terminal. J Physiol (Lond) 477: 437-448, 1994