The efferent medial olivocochlear-hair cell synapse

Journal of Physiology Paris

Volumn 106, Issue 1-2, 2012, Pages 47-56

  Elgoyhen, Ana Belén ^a,b   Katz, Eleonora ^a,b  

^a INSTITUTO DE INVESTIGACIONES EN INGENIERÍA GENÉTICA Y BIOLOGÍA MOLECULAR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

9 and 10 Nicotinic receptors; Cochlea; Hair cells; Nicotinic receptors; Prestin; SK channels; Synaptic plasticity

Indexed keywords

ACETYLCHOLINE; ION CHANNEL; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA10; NICOTINIC RECEPTOR ALPHA9; PRESTIN; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ARTICLE; AUDITORY STIMULATION; CALCIUM CELL LEVEL; CELL ACTIVATION; CELL FUNCTION; CELL INTERACTION; CELL MOTILITY; COCHLEAR NERVE; EFFERENT NERVE; HAIR CELL; HUMAN; HYPERPOLARIZATION; INTRACELLULAR SIGNALING; MEMBRANE PERMEABILITY; NERVE CELL INHIBITION; NERVE CELL PLASTICITY; NONHUMAN; OLIVARY NUCLEUS; OLIVOCOCHLEAR HAIR CELL; POTASSIUM CURRENT; SIGNAL PROCESSING; SOUND TRANSMISSION; SYNAPSE; SYNAPTIC TRANSMISSION; VIBRATION;

ANIMALS; COCHLEA; EFFERENT PATHWAYS; HAIR CELLS, AUDITORY; HUMANS; OLIVARY NUCLEUS; RECEPTORS, NICOTINIC; SYNAPSES;

EID: 84858190504     PISSN: 09284257     EISSN: 17697115     Source Type: Journal    
DOI: 10.1016/j.jphysparis.2011.06.001     Document Type: Article

References (167)

1. Albert J.T., Winter H., Schaechinger T.J., Weber T., Wang X., He D.Z., Hendrich O., Geisler H.S., Zimmermann U., Oelmann K., Knipper M., Gopfert M.C., Oliver D. Voltage-sensitive prestin orthologue expressed in zebrafish hair cells. J. Physiol. 2007, 580:451-461.
2. Art J., Fettiplace R., Fuchs P. Synaptic hyperpolarization and inhibition of turtle cochlear hair cells. J. Physiol. (Lond.) 1984, 365:525-550.
3. Ashmore J.F., Russell I.J. Sensory and effector functions of vertebrate hair cells. J. Submicrosc. Cytol. 1983, 15:163-166.
4. Ballestero J.A., Plazas P.V., Kracun S., Gomez-Casati M.E., Taranda J., Rothlin C.V., Katz E., Millar N.S., Elgoyhen A.B. Effects of quinine, quinidine, and chloroquine on alpha9alpha10 nicotinic cholinergic receptors. Mol. Pharmacol. 2005, 68:822-829.
5. + channels: from protein complexes to function. Physiol. Rev. 2010, 90:1437-1459.
6. Bertrand D., Galzi J., Devillers-Thiery A., Bertrand S., Changeux J. Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal α7 nicotinic receptor. Proc. Natl. Acad. Sci. USA 1993, 90:6971-6975.
7. Beutner D., Moser T. The presynaptic function of mouse cochlear inner hair cells during development of hearing. J. Neurosci. 2001, 21:4593-4599.
8. Blanchet C., Erostegui C., Sugasawa M., Dulon D. Acetylcholine-induced potassium current of guinea pig outer hair cells: its dependence on a calcium influx through nicotinic-like receptors. J. Neurosci. 1996, 16:2574-2584.
9. + channel knock-out mice reveal the identity of calcium-dependent after hyperpolarization currents. J. Neurosci. 2004, 24:5301-5306.
10. Borst J.G., Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature 1996, 383:431-434.
11. Boulter J., Evans K., Goldman D., Martin G., Treco D., Heinemann S., Patrick J. Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor α-subunit. Nature 1986, 319:368-374.
12. Boulter J., Connolly J., Deneris E., Goldman D., Heinemann S., Patrick J. Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family. Proc. Natl. Acad. Sci. USA 1987, 84:7763-7767.
13. Brigande J.V., Heller S. Quo vadis, hair cell regeneration?. Nat. Neurosci. 2009, 12:679-685.
14. Brownell W., Bader C., Bertrand D., de Ribaupierre Y. Evoked mechanical responses of isolated cochlear hair cells. Science 1985, 227:194-196.
15. Burnashev N., Schoepfer R., Monyer H., Ruppersberg J., Gunther W., Seeburg P., Sakmann B. Control by asparagine residues of calcium permeability and magnesium blockade in the NMDA receptor. Science 1992, 257:1415-1419.
16. Cabanillas L.A., Luebke A.E. CGRP- and cholinergic-containing fibers project to guinea pig outer hair cells. Hearing Res. 2002, 172:14-17.
17. Caulfield M.P., Birdsall N.J. International union of pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol. Rev. 1998, 50:279-290.
18. 2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat. Neurosci. 2005, 8:149-155.
19. Churchill J.A., Schuknecht H.F., Doran R. Acetylcholinesterase activity in the cochlea. Laryngoscope 1956, 66:1-15.
20. Couturier S., Bertrand D., Matter J.-M., Hernandez M.-C., Bertrand S., Millar N., Valera S., Barkas T., Ballivet M. A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 1990, 5:847-856.
21. Dallos P. Cochlear amplification, outer hair cells and prestin. Curr. Opin. Neurobiol. 2008, 18:370-376.
22. Dannhof B.J., Roth B., Bruns V. Anatomical mapping of choline acetyltransferase (ChAT)-like and glutamate decarboxylase (GAD)-like immunoreactivity in outer hair cell efferents in adult rats. Cell Tissue Res. 1991, 266:89-95.
23. Delano P.H., Elgueda D., Hamame C.M., Robles L. Selective attention to visual stimuli reduces cochlear sensitivity in chinchillas. J. Neurosci. 2007, 27:4146-4153.
24. Deneris E.S., Connolly J., Boulter J., Wada E., Wada K., Swanson L.W., Patrick J., Heinemann S. Primary structure and expression of β2: a novel subunit of neuronal nicotinic acetylcholine receptors. Neuron 1988, 1:45-54.
25. Dent J.A. Evidence for a diverse Cys-loop ligand-gated ion channel superfamily in early Bilateria. J. Mol. Evol. 2006, 62:523-535.
26. Dodge F.A., Rahamimoff R. On the relationship between calcium concentration and the amplitude of the end-plate potential. J. Physiol. 1967, 189:90P-92P.
27. 2+ concentration and hyperpolarizes the guinea-pig outer hair cell. Hearing Res. 1993, 67:179-188.
28. Dolan D.F., Nuttall A.L. Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. J. Acoust. Soc. Am. 1988, 83:1081-1086.
29. Dulon D., Lenoir M. Cholinergic responses in developing outer hair cells of the rat cochlea. Eur. J. Neurosci 1996, 8:1945-1952.
30. Dulon D., Luo L., Zhang C., Ryan A.F. Expression of small-conductance calcium-activated potassium channels (SK) in outer hair cells of the rat cochlea. Eur. J. Neurosci. 1998, 10:907-915.
31. Duvoisin R.M., Deneris E.S., Patrick J., Heinemann S. The functional diversity of the neuronal nicotinic acetylcholine receptors is increased by a novel subunit: β4. Neuron 1989, 3:487-496.
32. 2+ permeation in cyclic nucleotide-gated channels. EMBO J. 1999, 18:131-144.
33. Eggermont J.J., Roberts L.E. The neuroscience of tinnitus. Trends Neurosci. 2004, 27:676-682.
34. Elgoyhen A.B., Franchini L.F. Prestin and the cholinergic receptor of hair cells: positively-selected proteins in mammals. Hearing Res. 2011, 273:100-108.
35. Elgoyhen A.B., Langguth B. Pharmacological approaches to the treatment of tinnitus. Drug Discov. Today 2010, 15:300-305.
36. Elgoyhen A.B., Johnson D.S., Boulter J., Vetter D.E., Heinemann S. A9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 1994, 79:705-715.
37. Elgoyhen A.B., Vetter D., Katz E., Rothlin C., Heinemann S., Boulter J. Alpha 10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. PNAS, USA 2001, 98:3501-3506.
38. Elgoyhen A.B., Katz E., Fuchs P.A. The nicotinic receptor of cochlear hair cells: a possible pharmacotherapeutic target?. Biochem. Pharmacol. 2009, 78:712-719.
39. Ellison M., Haberlandt C., Gomez-Casati M.E., Watkins M., Elgoyhen A.B., McIntosh J.M., Olivera B.M. Alpha-RgIA: a novel conotoxin that specifically and potently blocks the alpha9alpha10 nAChR. Biochemistry 2006, 45:1511-1517.
40. Erostegui C., Norris C.H., Bobbin R.P. In vitro characterization of a cholinergic receptor on outer hair cells. Hearing Res. 1994, 74:135-147.
41. Evans M. Acetylcholine activates two currents in guinea-pig outer hair cells. J. Physiol. 1996, 491:563-578.
42. Eybalin M. Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol. Rev. 1993, 73:309-373.
43. Eybalin M., Altschuler R.A. Immunoelectron microscopic localization of neurotransmitters in the cochlea. J. Electron Microsc. Tech. 1990, 15:209-224.
44. Eybalin M., Pujol R. Choline acetyltransferase (ChAT) immunoelectron microscopy distinguishes at least three types of efferent synapses in the organ of Corti. Exp. Brain Res. 1987, 65:261-270.
45. Fedchyshyn M.J., Wang L.Y. Developmental transformation of the release modality at the calyx of Held synapse. J. Neurosci. 2005, 25:4131-4140.
46. + channels induces dihydropyridine sensitivity of ACh release from mammalian motor nerve terminals. J. Pharmacol. Exp. Ther. 2003, 305:646-652.
47. Flock A., Russell I.J. The post-synaptic action of efferent fibres in the lateral line organ of the burbot Lota lota. J. Physiol. 1973, 235:591-605.
48. Franchini L.F., Elgoyhen A.B. Adaptive evolution in mammalian proteins involved in cochlear outer hair cell electromotility. Mol. Phylogen. Evol. 2006, 41:622-635.
49. Fuchs P. Synaptic transmission at vertebrate hair cells. Curr. Opin. Neurobiol. 1996, 6:514-519.
50. Fuchs P.A., Murrow B.W. Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J. Neurosci. 1992, 12:800-809.
51. Fuchs P.A., Murrow B.W. A novel cholinergic receptor mediates inhibition of chick cochlear hair cells. Proc. Roy. Soc. Lond. Ser. B 1992, 248:35-40.
52. Galambos R. Suppression of auditory nerve activity by stimulation of efferent fibers to the cochlea. J. Neurophysiol. 1956, 19:424-437.
53. Gifford M.L., Guinan J.J. Effects of electrical stimulation of medial olivocochlear neurons on ipsilateral and contralateral cochlear responses. Hearing Res. 1987, 29:179-194.
54. Glowatzki E., Fuchs P. Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 2000, 288:2366-2368.
55. Glowatzki E., Fuchs P. Transmitter release at the hair cell ribbon synapse. Nat. Neurosci. 2002, 5:147-154.
56. Glowatzki E., Wild K., Brandle U., Fakler G., Fakler B., Zenner H.P., Ruppersberg J.P. Cell-specific expression of the alpha 9 n-ACh receptor subunit in auditory hair cells revealed by single-cell RT-PCR. Proc. Roy. Soc. Lond. Ser. B 1995, 262:141-147.
57. Gomez-Casati M.E., Fuchs P.A., Elgoyhen A.B., Katz E. Biophysical and pharmacological characterization of nicotinic cholinergic receptors in cochlear inner hair cells. J. Physiol. 2005, 566:103-118.
58. Goutman J.D., Fuchs P.A., Glowatzki E. Facilitating efferent inhibition of inner hair cells in the cochlea of the neonatal rat. J. Physiol. 2005, 566:49-59.
59. Guinan J.J. Physiology of Olivocochlear Efferents. The Cochlea. Dallos, Popper and Fay 1996, Springer-Verlag, New York, pp. 435-502.
60. Guinan J.J., Warr W.B., Norris B.E. Differential olivocochlear projections from lateral vs medial zones of the superior olivary complex. J. Comput. Neurol. 1983, 221:358-370.
61. Gulley R.L., Reese T.S. Freeze-fracture studies on the synapses in the organ of Corti. J. Comput. Neurol. 1977, 171:517-543.
62. He D.Z., Cheatham M.A., Pearce M., Vetter D.E. Mouse outer hair cells lacking the alpha9 ACh receptor are motile. Brain Res. Dev. Brain Res. 2004, 148:19-25.
63. Hiel H., Elgoyhen A., Drescher D., Morley B. Expression of nicotinic acetylcholine receptor mRNA in the adult rat peripheral vestibular system. Brain Res. 1996, 738:347-352.
64. Hiel H., Luebke A.E., Fuchs P.A. Cloning and expression of the alpha9 nicotinic acetylcholine receptor subunit in cochlear hair cells of the chick. Brain Res. 2000, 858:215-225.
65. Hirokawa N. The ultrastructure of the basilar papilla of the chick. J. Comput. Neurol. 1978, 181:361-374.
66. Housley G.D., Ashmore J.F. Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc. Roy. Soc. Lond. Ser. B 1991, 244:161-167.
67. Hudspeth A. How hearing happens. Neuron 1997, 19:947-950.
68. Hudspeth A.J. Making an effort to listen: mechanical amplification in the ear. Neuron 2008, 59:530-545.
69. Jia S., He D.Z. Motility-associated hair-bundle motion in mammalian outer hair cells. Nat. Neurosci. 2005, 8:1028-1034.
70. 2+ dependence of exocytosis. J. Physiol. 2007, 583:631-646.
71. Kakehata S., Nakagawa T., Takasaka T., Akaike N. Cellular mechanism of acetylcholine-induced response in dissociated outer hair cells of guinea-pig cochlea. J. Physiol. (Lond.) 1993, 463:227-244.
72. Karlin A. Ion channel structure: emerging structure of the nicotinic acetylcholine receptors. Nat. Rev. Neurosci. 2002, 3:102-114.
73. Karlin A., Akabas M. Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 1995, 15:1231-1244.
74. Katz E., Verbitsky M., Rothlin C., Vetter D., Heinemann S., Elgoyhen A. High calcium permeability and calcium block of the α9 nicotinic acetylcholine receptor. Hearing Res. 2000, 141:117-128.
75. Katz E., Elgoyhen A.B., Gomez-Casati M.E., Knipper M., Vetter D.E., Fuchs P.A., Glowatzki E. Developmental regulation of nicotinic synapses on cochlear inner hair cells. J. Neurosci. 2004, 24:7814-7820.
76. Kawase T., Delgutte B., Liberman M.C. Antimasking effects of the olivocochlear reflex. II. Enhancement of auditory-nerve response to masked tones. J. Neurophysiol. 1993, 70:2533-2549.
77. Kennedy H.J., Crawford A.C., Fettiplace R. Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 2005, 433:880-883.
78. Kong J.H., Adelman J.P., Fuchs P.A. Expression of the SK2 calcium-activated potassium channel is required for cholinergic function in mouse cochlear hair cells. J. Physiol. 2008, 586:5471-5485.
79. Kujawa S.G., Glattke T.J., Fallon M., Bobbin R. A nicotinic-like receptor mediates suppression of distortion product otoacustic emissions by contralateral sound. Hearing Res. 1994, 74:122-134.
80. Kuriyama H., Shiosaka S., Sekitani M., Tohyama Y., Kitajiri M., Yamashita T., Kumazawa T., Tohyama M. Electron microscopic observation of calcitonin gene-related peptide-like immunoreactivity in the organ of Corti of the rat. Brain Res. 1990, 517:76-80.
81. Le Novere N., Changeux J. Molecular evolution of the nicotinic acetylcholine receptor: an example of multigene family in excitable cells. J. Mol. Evol. 1995, 40:155-172.
82. Le Novere N., Corringer P.J., Changeux J.P. The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J. Neurobiol. 2002, 53:447-456.
83. Liberman M.C. The olivocochlear efferent bundle and susceptibility of the inner ear to acoustic injury. J. Neurophysiol. 1991, 65:123-132.
84. Lim D.J. Effects of noise and ototoxic drugs at the cellular level in the cochlea: a review. Am. J. Otolaryngol. 1986, 7:73-99.
85. Lioudyno M., Verbitsky M., Holt J., Elgoyhen A., Guth P. Morphine inhibits an a9-acetylcholine nicotinic receptor-mediated response by a mechanism which does not involve opioid receptors. Hearing Res. 2000, 149:167-177.
86. Lioudyno M.I., Verbitsky M., Glowatzki E., Holt J.C., Boulter J., Zadina J.E., Elgoyhen A.B., Guth P.S. The alpha9/alpha10-containing nicotinic ACh receptor is directly modulated by opioid peptides, endomorphin-1, and dynorphin B, proposed efferent cotransmitters in the inner ear. Mol. Cell. Neurosci. 2002, 20:695-711.
87. Lioudyno M., Hiel H., Kong J.H., Katz E., Waldman E., Parameshwaran-Iyer S., Glowatzki E., Fuchs P.A. A " synaptoplasmic cistern" mediates rapid inhibition of cochlear hair cells. J. Neurosci. 2004, 24:11160-11164.
88. Lukas R.J., Changeux J.P., Le Novere N., Albuquerque E.X., Balfour D.J., Berg D.K., Bertrand D., Chiappinelli V.A., Clarke P.B., Collins A.C., Dani J.A., Grady S.R., Kellar K.J., Lindstrom J.M., Marks M.J., Quik M., Taylor P.W., Wonnacott S. International Union of Pharmacology. XX. Current status of the nomenclature for nicotinic acetylcholine receptors and their subunits. Pharmacol. Rev. 1999, 51:397-401.
89. Lustig L., Hiel H., Fuchs P. Vestibular hair cells of the chick express the nicotinic acetylcholine receptor subunit alpha9. J. Vestib. Res. 1999, 9:359-367.
90. Lustig L.R., Peng H., Hiel H., Yamamoto T., Fuchs P. Molecular cloning and mapping of the human nicotinic acetylcholine receptor α10 (CHRNA10). Genomics 2001, 73:272-283.
91. Maison S.F., Liberman M.C. Predicting vulnerability to acoustic injury with a noninvasive assay of olivocochlear reflex strength. J. Neurosci. 2000, 20:4701-4707.
92. Maison S.F., Luebke A.E., Liberman M.C., Zuo J. Efferent protection from acoustic injury is mediated via alpha9 nicotinic acetylcholine receptors on outer hair cells. J. Neurosci. 2002, 22:10838-10846.
93. Maison S.F., Adams J.C., Liberman M.C. Olivocochlear innervation in the mouse: immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. J. Comput. Neurol. 2003, 455:406-416.
94. Maison S.F., Emeson R.B., Adams J.C., Luebke A.E., Liberman M.C. Loss of alpha CGRP reduces sound-evoked activity in the cochlear nerve. J. Neurophysiol. 2003, 90:2941-2949.
95. Maison S.F., Rosahl T.W., Homanics G.E., Liberman M.C. Functional role of GABAergic innervation of the cochlea: phenotypic analysis of mice lacking GABA(A) receptor subunits alpha 1, alpha 2, alpha 5, alpha 6, beta 2, beta 3, or delta. J. Neurosci. 2006, 26:10315-10326.
96. Maison S.F., Parker L.L., Young L., Adelman J.P., Zuo J., Liberman M.C. Overexpression of SK2 channels enhances efferent suppression of cochlear responses without enhancing noise resistance. J. Neurophysiol. 2007, 97:2930-2936.
97. Manley G.A., Koppl C. Phylogenetic development of the cochlea and its innervation. Curr. Opin. Neurobiol. 1998, 8:468-474.
98. Marcantoni A., Baldelli P., Hernandez-Guijo J.M., Comunanza V., Carabelli V., Carbone E. L-type calcium channels in adrenal chromaffin cells: role in pace-making and secretion. Cell Calcium 2007, 42:397-408.
99. Marcotti W., Johnson S.L., Kros C.J. Effects of intracellular stores and extracellular Ca(2+) on Ca(2+)-activated K(+) currents in mature mouse inner hair cells. J. Physiol. 2004, 557:613-633.
100. Marcotti W., Johnson S.L., Kros C.J. A transiently expressed SK current sustains and modulates action potential activity in immature mouse inner hair cells. J. Physiol. 2004, 560:691-708.
101. May B.J., Prosen C.A., Weiss D., Vetter D. Behavioral investigation of some possible effects of the central olivocochlear pathways in transgenic mice. Hearing Res. 2002, 171:142-157.
102. Mayer M., Westbrook G. Permeation and block of N-methyl-d-aspartic acid receptor channels by divalent cations in mouse cultured central neurones. J. Physiol. (Lond.) 1987, 394:501-527.
103. McIntosh J.M., Plazas P.V., Watkins M., Gomez-Casati M.E., Olivera B.M., Elgoyhen A.B. A novel alpha-conotoxin, PeIA, cloned from Conus pergrandis, discriminates between rat alpha9alpha10 and alpha7 nicotinic cholinergic receptors. J. Biol. Chem. 2005, 280:30107-30112.
104. McIntosh J.M., Absalom N., Chebib M., Elgoyhen A.B., Vincler M. Alpha9 nicotinic acetylcholine receptors and the treatment of pain. Biochem. Pharmacol. 2009, 78:693-702.
105. McNiven A.I., Yuhas W.A., Fuchs P.A. Ionic dependence and agonist preference of an acetylcholine receptor in hair cells. Audit. Neurosci. 1996, 2:63-77.
106. Mintz I.M., Sabatini B.L., Regehr W.G. Calcium control of transmitter release at a cerebellar synapse. Neuron 1995, 15:675-688.
107. Morley B., Li H., Hiel H., Drescher D., Elgoyhen A.B. Identification of the subunits of the nicotinic cholinergic receptors in the rat cochlea using RT-PCR and in situ hybridization. Mol. Brain Res. 1998, 53:78-87.
108. Moroni M., Bermudez I. Stoichiometry and pharmacology of two human alpha4beta2 nicotinic receptor types. J. Mol. Neurosci. 2006, 30:95-96.
109. Mount D.B., Romero M.F. The SLC26 gene family of multifunctional anion exchangers. Pflugers Arch. 2004, 447:710-721.
110. Murthy V., Maison S.F., Taranda J., Haque N., Bond C.T., Elgoyhen A.B., Adelman J.P., Liberman M.C., Vetter D.E. SK2 channels are required for function and long-term survival of efferent synapses on mammalian outer hair cells. Mol. Cell. Neurosci. 2009, 40:39-49.
111. Murthy V., Taranda J., Elgoyhen A.B., Vetter D.E. Activity of nAChRs containing alpha9 subunits modulates synapse stabilization via bidirectional signaling programs. Dev. Neurobiol. 2009, 69:931-949.
112. Murugasu E., Russell I.J. The effect of efferent stimulation on basilar membrane displacement in the basal turn of the guinea pig cochlea. J. Neurosci. 1996, 16:325-332.
113. Nenov A.P., Norris C., Bobbin R.P. Acetylcholine response in guinea pig outer hair cells. I. Properties of the response. Hearing Res. 1996, 101:132-148.
114. + channel. Hearing Res. 1996, 101:149-172.
115. Nevin S.T., Clark R.J., Klimis H., Christie M.J., Craik D.J., Adams D.J. Are alpha9alpha10 nicotinic acetylcholine receptors a pain target for alpha-conotoxins?. Mol. Pharmacol. 2007, 72:1406-1410.
116. Oatman L.C. Effects of visual attention on the intensity of auditory evoked potentials. Exp. Neurol. 1976, 51:41-53.
117. + channels controls fast inhibitory synaptic transmission at auditory outer hair cells. Neuron 2000, 26:595-601.
118. Plazas, P., Katz, E., Elgoyhen, A., 2002. Unconventional properties of an a9a10 nicotinic receptor mutated in the Leu9' of the channel domain. 32nd Annual Meeting, Society for Neuroscience, Orlando, USA, 2002.
119. Plazas P.V., Katz E., Gomez-Casati M.E., Bouzat C., Elgoyhen A.B. Stoichiometry of the {alpha}9{alpha}10 Nicotinic Cholinergic Receptor. J. Neurosci. 2005, 25:10905-10912.
120. Plazas P.V., Savino J., Kracun S., Gomez-Casati M.E., Katz E., Parsons C.G., Millar N.S., Elgoyhen A.B. Inhibition of the alpha9alpha10 nicotinic cholinergic receptor by neramexane, an open channel blocker of N-methyl-d-aspartate receptors. Eur. J. Pharmacol. 2007, 566:11-19.
121. Rajan R. Centrifugal pathways protect hearing sensitivity at the cochlea in noisy environments that exacerbate the damage induced by loud sound. J. Neurosci. 2000, 6684:6693.
122. Rasmussen G.L. The olivary peduncle and other fiber projections of the superior olivary complex. J. Comput. Neurol. 1946, 84:141-219.
123. 2+ channels: a functional patchwork. Trends Neurosci. 2003, 26:683-687.
124. Reiter E.R., Liberman M.C. Efferent-mediated protection from acoustic overexposure: relation to slow effects of olivocochlear stimulation. J. Neurophysiol. 1995, 73:506-514.
125. Rothlin C., Verbitsky M., Katz E., Elgoyhen A. The α9 nicotinic acetylcholine receptor shares pharmacological properties with type A γ-aminobutyric acid, glycine and type 3 serotonin receptors. Mol. Pharmacol. 1999, 55:248-254.
126. Rothlin C.V., Katz E., Verbitsky M., Vetter D., Heinemann S., Elgoyhen A.B. Block of the α9 nicotinic receptor by ototoxic aminoglycosides. Neuropharmacology 2000, 39:2525-2532.
127. Rothlin C.V., Lioudyno M.I., Silbering A.F., Plazas P.V., Casati M.E., Katz E., Guth P.S., Elgoyhen A.B. Direct interaction of serotonin type 3 receptor ligands with recombinant and native alpha 9 alpha 10-containing nicotinic cholinergic receptors. Mol. Pharmacol. 2003, 63:1067-1074.
128. Russell I.J., Murugasu E. Medial efferent inhibition suppresses basilar membrane responses to near characteristic frequency tones of moderate to high intensities. J. Acoust. Soc. Am. 1997, 102:1734-1738.
129. Saito K. Fine structure of the sensory epithelium of guinea-pig organ of Corti: subsurface cisternae and lamellar bodies in the outer hair cells. Cell Tissue Res. 1983, 229:467-481.
130. Schaechinger T.J., Oliver D. Nonmammalian orthologs of prestin (SLC26A5) are electrogenic divalent/chloride anion exchangers. Proc. Natl. Acad. Sci. USA 2007, 104:7693-7698.
131. Schoepfer R., Conroy W.G., Whiting P., Gore M., Lindstrom J. Brain α-bungarotoxin binding protein cDNAs and Mabs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 1990, 5:35-48.
132. Schuknecht H.F., Churchill J.A., Doran R. The localization of acetylcholinesterase in the cochlea. AMA Arch. Otolaryngol. 1959, 69:549-559.
133. Séguéla P., Wadiche J., Dineley-Miller K., Dani J.A., Patrick J.W. Molecular cloning, functional properties, and distribution of rat brain α7: a nicotinic cation channel highly permeable to calcium. J. Neurosci. 1993, 13:596-604.
134. Sgard F., Charpentier E., Bertrand S., Walker N., Caput D., Graham D., Bertrand D., Besnard F. A novel human nicotinic receptor subunit, α10, that confers functionality to the α9-subunit. Mol. Pharmacol. 2002, 61:150-159.
135. 2+ concentration in chick cochlear hair cells. J. Physiol. (Lond.) 1990, 420:127-148.
136. + channels. J. Physiol. 1991, 442:669-690.
137. Simmons D.D. Development of the inner ear efferent system across vertebrate species. J. Neurobiol. 2002, 53:228-250.
138. Simmons D.D., Morley B.J. Differential expression of the alpha 9 nicotinic acetylcholine receptor subunit in neonatal and adult cochlear hair cells. Brain Res. Mol. Brain Res. 1998, 56:287-292.
139. Storm J.F. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J. Physiol. 1987, 385:733-759.
140. Suckfull M., Althaus M., Ellers-Lenz B., Gebauer A., Gortelmeyer R., Jastreboff P.J., Moebius H.J., Rosenberg T., Russ H., Wirth Y., Krueger H. A randomized, double-blind, placebo-controlled clinical trial to evaluate the efficacy and safety of neramexane in patients with moderate to severe subjective tinnitus. BMC Ear Nose Throat Disord. 2011, 11:1.
141. Sugai T., Yano J., Sugitani M., Ooyama H. Actions of cholinergic agonists and antagonists on the efferent synapse in the frog sacculus. Hearing Res. 1992, 61:56-64.
142. Tan X., Pecka J.L., Tang J., Okoruwa O.E., Zhang Q., Beisel K.W., He D.Z. From zebrafish to mammal: functional evolution of prestin, the motor protein of cochlear outer hair cells. J. Neurophysiol. 2011, 105:36-44.
143. Taranda J., Ballestero J.A., Hiel H., de Souza F.S., Wedemeyer C., Gomez-Casati M.E., Lipovsek M., Vetter D.E., Fuchs P.A., Katz E., Elgoyhen A.B. Constitutive expression of the alpha10 nicotinic acetylcholine receptor subunit fails to maintain cholinergic responses in inner hair cells after the onset of hearing. J. Assoc. Res. Otolaryngol. 2009, 10:397-406.
144. Taranda J., Maison S.F., Ballestero J.A., Katz E., Savino J., Vetter D.E., Boulter J., Liberman M.C., Fuchs P.A., Elgoyhen A.B. A point mutation in the hair cell nicotinic cholinergic receptor prolongs cochlear inhibition and enhances noise protection. PLoS Biol. 2009, 7:e18.
145. Tohyama Y., Kiyama H., Kitajiri M., Yamashita T., Kumazawa T., Tohyama M. Ontogeny of calcitonin gene-related peptide in the organ of Corti of the rat. Brain Res. Dev. Brain Res. 1989, 45:309-312.
146. Tritsch N.X., Bergles D.E. Developmental regulation of spontaneous activity in the Mammalian cochlea. J. Neurosci. 2010, 30:1539-1550.
147. Tritsch N.X., Yi E., Gale J.E., Glowatzki E., Bergles D.E. The origin of spontaneous activity in the developing auditory system. Nature 2007, 450:50-55.
148. Tritsch N.X., Rodriguez-Contreras A., Crins T.T., Wang H.C., Borst J.G., Bergles D.E. Calcium action potentials in hair cells pattern auditory neuron activity before hearing onset. Nat. Neurosci. 2010, 13:1050-1052.
149. Tsunoyama K., Gojobori T. Evolution of nicotinic acetylcholine receptor subunits. Mol. Biol. Evol. 1998, 15:518-527.
150. Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 2005, 346:967-989.
151. Urbano F.J., Depetris R.S., Uchitel O.D. Coupling of L-type calcium channels to neurotransmitter release at mouse motor nerve terminals. Pflugers Arch. 2001, 441:824-831.
152. Verbitsky M., Rothlin C., Katz E., Elgoyhen A.B. Mixed nicotinic-muscarinic properties of the a9 nicotinic cholinergic receptor. Neuropharmacology 2000, 39:2515-2524.
153. Vetter D., Lieberman M., Mann J., Barhanin J., Boulter J., Brown M., Saffiote-Kollman J., Heinemann S., Elgoyhen A. Role of a9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 1999, 23:93-103.
154. Vetter D.E., Katz E., Maison S.F., Taranda J., Turcan S., Ballestero J., Liberman M.C., Elgoyhen A.B., Boulter J. The alpha10 nicotinic acetylcholine receptor subunit is required for normal synaptic function and integrity of the olivocochlear system. Proc. Natl. Acad. Sci. USA 2007, 104:20594-20599.
155. Wada K., Ballivet M., Boulter J., Connolly J., Wada E., Deneris E.S., Swanson L.W., Heinemann S.F., Patrick J. Functional expression of a new pharmacological subtype of brain nicotinic acetylcholine receptor. Science 1988, 240:330-334.
156. Warr W.B. Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J. Comput. Neurol. 1975, 161:159-181.
157. Warr W. Organization of olivocochlear efferent systems in mammals. The Mammalian Auditory Pathway: Neuroanatomy 1992, 410-448. Springer-Verlag, New York. W. Douglas, A. Popper, R. Fay (Eds.).
158. Weber T., Gopfert M.C., Winter H., Zimmermann U., Kohler H., Meier A., Hendrich O., Rohbock K., Robert D., Knipper M. Expression of prestin-homologous solute carrier (SLC26) in auditory organs of nonmammalian vertebrates and insects. Proc. Natl. Acad. Sci. USA 2003, 100:7690-7695.
159. Weisstaub N., Vetter D., Elgoyhen A., Katz E. The alpha9/alpha10 nicotinic acetylcholine receptor is permeable to and is modulated by divalent cations. Hearing Res. 2002, 167:122-135.
160. Wersinger E., McLean W.J., Fuchs P.A., Pyott S.J. BK channels mediate cholinergic inhibition of high frequency cochlear hair cells. PLoS ONE 2011, 5:e13836.
161. Wiederhold M.L., Kiang N.Y.S. Effects of electrical stimulation of the crossed olivocochlear bundle on cat single auditory nerve fibres. J. Acoust. Soc. Am. 1970, 48:950-965.
162. Winslow R.L., Sachs M.B. Single-tone intensity discrimination based on auditory-nerve rate responses in backgrounds of quiet, noise, and with stimulation of the crossed olivocochlear bundle. Hearing Res. 1988, 35:165-189.
163. Yoshida N., Shigemoto T., Sugai T., Ohmori H. The role of inositol triphosphate on ACh-induced outward currents in bullfrog saccular hair cells. Brain Res. 1994, 644.
164. Yuhas W.A., Fuchs P.A. Apamin-sensitive, small-conductance, calcium-activated potassium channels mediate cholinergic inhibition of chick auditory hair cells. J. Comput. Physiol. [A] 1999, 185:455-462.
165. Zheng J., Shen W., He D.Z., Long K.B., Madison L.D., Dallos P. Prestin is the motor protein of cochlear outer hair cells. Nature 2000, 405:149-155.
166. Zorrilla de San Martin J., Ballestero J., Katz E., Elgoyhen A.B., Fuchs P.A. Ryanodine is a positive modulator of acetylcholine receptor gating in cochlear hair cells. J. Assoc. Res. Otolaryngol. 2007, 8:474-483.
167. Zorrilla de San Martin J., Pyott S., Ballestero J., Katz E. Ca(2+) and Ca(2+)-activated K(+) channels that support and modulate transmitter release at the olivocochlear efferent-inner hair cell synapse. J. Neurosci. 2010, 30:12157-12167.