Cholinergic Inhibition of Hair Cells

  • Eleonora Katz
  • Ana Belén Elgoyhen
  • Paul Albert Fuchs
Chapter
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 38)

Abstract

In the inner ear, the activity of hair cells that transform sound into electrical signals is modulated by a descending efferent innervation from the brain. A major component of this feedback involves cholinergic inhibition of hair cells via an unusual ionic mechanism. It activates rapidly (on the order of milliseconds), but instead of being mediated by a hyperpolarizing conductance through γ-aminobutyric acid (GABA) and/or glycine receptors, it is served by nicotinic cholinergic receptors (nAChR), which usually mediate excitatory postsynaptic responses. How is fast inhibition accomplished if the activation of a cationic channel (the nAChR) at the resting membrane potential should depolarize the hair cell?

Keywords

Permeability Glycine Nicotine Cysteine Choline 

References

  1. Alger BE (1991) Gating of GABAergic inhibition in hippocampal pyramidal cells. Ann NY Acad Sci 627:249–263PubMedGoogle Scholar
  2. Altschuler RA, Parakkal MH, Fex J (1983) Localization of enkephalin-like immunoreactivity in acetylcholinesterase-positive cells in the guinea-pig lateral superior olivary complex that project to the cochlea. Neuroscience 9:621–630PubMedGoogle Scholar
  3. Altschuler RA, Fex J, Parakkal MH, Eckenstein F (1984) Colocalization of enkephalin-like and choline acetyltransferase-like immunoreactivities in olivochoclear neurons of the guinea pig. J Histochem Cytochem 32:839–843PubMedGoogle Scholar
  4. Altschuler RA, Hoffman DW, Reeks KA, Fex J (1985) Localization of dynorphin B-like and alpha-neoendorphin-like immunoreactivities in the guinea pig organ of Corti. Hear Res 17:249–258PubMedGoogle Scholar
  5. Anderson AD, Troyanovskaya M, Wackym PA (1997) Differential expression of a2–7 and b2–4 nicotinic acetylcholine receptor subunit mRNA in the vestibular end-organs and Scarpa’s ganglia of the rat. Brain Res 778:409–413PubMedGoogle Scholar
  6. Art JJ, Fettiplace R (1984) Efferent desensitization of auditory nerve fibre responses in the cochlea of the turtle Pseudemys scripta elegans. J Physiol (Lond) 356:507–523Google Scholar
  7. Art JJ, Crawford AC, Fettiplace R, Fuchs PA (1982) Efferent regulation of hair cells in the turtle cochlea. Proc R Soc Lond B Biol Sci 216:377–384PubMedGoogle Scholar
  8. Art JJ, Fettiplace R, Fuchs PA (1984) Synaptic hyperpolarization and inhibition of turtle cochlear hair cells. J Physiol (Lond) 356:525–550Google Scholar
  9. Art JJ, Crawford AC, Fettiplace R, Fuchs PA (1985) Efferent modulation of hair cell tuning in the cochlea of the turtle. J Physiol (Lond) 360:397–421Google Scholar
  10. Ashmore JF (1983) Frequency tuning in a frog vestibular organ. Nature 304:536–538PubMedGoogle Scholar
  11. Betz H, Kuhse J, Schmieden V, Laube B, Kirsch J, Harvey RJ (1999) Structure and functions of inhibitory and excitatory glycine receptors. Ann NY Acad Sci 868:667–676PubMedGoogle Scholar
  12. Beutner D, Moser T (2001) The presynaptic function of mouse cochlear inner hair cells during development of hearing. J Neurosci 21:4593–4599PubMedGoogle Scholar
  13. Blanchet C, Erostegui C, Sugasawa M, Dulon D (1996) Acetylcholine-induced potassium current of guinea pig outer hair cells: its dependence on a calcium influx through nicotinic-like receptors. J Neurosci 16:2574–2584PubMedGoogle Scholar
  14. Bond CT, Herson PS, Strassmaier T, Hammond R, Stackman R, Maylie J, Adelman JP (2004) Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci 24:5301–5306PubMedGoogle Scholar
  15. Cabanillas LA, Luebke AE (2002) CGRP- and cholinergic-containing fibers project to guinea pig outer hair cells. Hear Res 172:14–17PubMedGoogle Scholar
  16. Cabello N, Remelli R, Canela L, Soriguera A, Mallol J, Canela EI, Robbins MJ, Lluis C, Franco R, McIlhinney RA, Ciruela F (2007) Actin-binding protein alpha-actinin-1 interacts with the metabotropic glutamate receptor type 5b and modulates the cell surface expression and function of the receptor. J Biol Chem 282:12143–12153PubMedGoogle Scholar
  17. Delano PH, Elgueda D, Hamame CM, Robles L (2007) Selective attention to visual stimuli reduces cochlear sensitivity in chinchillas. J Neurosci 27:4146–4153PubMedGoogle Scholar
  18. Dolan DF, Nuttall AL (1988) Masked cochlear whole-nerve response intensity functions altered by electrical stimulation of the crossed olivocochlear bundle. J Acoust Soc Am 83:1081–1086PubMedGoogle Scholar
  19. Dulon D, Lenoir M (1996) Cholinergic responses in developing outer hair cells of the rat cochlea. Eur J Neurosci 8:1945–1952PubMedGoogle Scholar
  20. Dulon D, Luo L, Zhang C, Ryan AF (1998) Expression of small-conductance calcium-activated potassium channels (SK) in outer hair cells of the rat cochlea. Eur J Neurosci 10:907–915PubMedGoogle Scholar
  21. Elgoyhen AB, Johnson DS, Boulter J, Vetter DE, Heinemann S (1994) Alpha 9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 79:705–715PubMedGoogle Scholar
  22. Elgoyhen A, Vetter D, Katz E, Rothlin C, Heinemann S, Boulter J (2001) Alpha 10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci USA 98:3501–3506PubMedGoogle Scholar
  23. Evans MG (1996) Acetylcholine activates two currents in guinea-pig outer hair cells. J Physiol (Lond) 491:563–578Google Scholar
  24. Eybalin M (1993) Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol Rev 73:309–373PubMedGoogle Scholar
  25. Eybalin M, Parnaud C, Geffard M, Pujol R (1988) Immunoelectron microscopy identifies several types of GABA-containing efferent synapses in the guinea-pig organ of Corti. Neuroscience 24:29–38PubMedGoogle Scholar
  26. Fex J, Altschuler RA (1981) Enkephalin-like immunoreactivity of olivochoclear nerve fibers in cochlea of guinea pig and cat. Proc Natl Acad Sci USA 78:1255–1259PubMedGoogle Scholar
  27. Flock A (1983) Hair cells, receptors with a motor capacity? In: Klinke R, Hartmann R (eds) Hearing-physiological bases and psychophysics. Springer, Berlin, pp 2–8Google Scholar
  28. Flock A, Russell I (1976) Inhibition by efferent nerve fibres: action on hair cells and afferent synaptic transmission in the lateral line canal organ of the burbot Lota lota. J Physiol 257:45–62PubMedGoogle Scholar
  29. Franchini LF, Elgoyhen AB (2006) Adaptive evolution in mammalian proteins involved in cochlear outer hair cell electromotility. Mol Phylogenet Evol 41:622–635PubMedGoogle Scholar
  30. Fuchs PA (1996) Synaptic transmission at vertebrate hair cells. Curr Opin Neurobiol 6:514–519PubMedGoogle Scholar
  31. Fuchs PA, Evans MG (1990) Potassium currents in hair cells isolated from the cochlea of the chick. J Physiol (Lond) 429:529–551Google Scholar
  32. Fuchs PA, Murrow BW (1992a) A novel cholinergic receptor mediates inhibition of chick cochlear hair cells. Proc R Soc Lond B Biol Sci 248:35–40Google Scholar
  33. Fuchs PA, Murrow BW (1992b) Cholinergic inhibition of short (outer) hair cells of the chick’s cochlea. J Neurosci 12:800–809PubMedGoogle Scholar
  34. Galambos R (1956) Suppression of auditory nerve activity by stimulation of efferent fibers to cochlea. J Neurophysiol 19:424–437PubMedGoogle Scholar
  35. Glowatzki E, Fuchs PA (2000) Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 288:2366–2368PubMedGoogle Scholar
  36. Gomez-Casati ME, Fuchs PA, Elgoyhen AB, Katz E (2005) Biophysical and pharmacological characterization of nicotinic cholinergic receptors in rat cochlear inner hair cells. J Physiol 566:103–118PubMedGoogle Scholar
  37. Goutman JD, Fuchs PA, Glowatzki E (2005) Facilitating efferent inhibition of inner hair cells in the cochlea of the neonatal rat. J Physiol 566:49–59PubMedGoogle Scholar
  38. Guinan JJ (1996) Efferent physiology. In: Dallos P, Popper AN, Fay RR (eds) The cochlea. Springer, New York, pp 435–502Google Scholar
  39. Guinan JJ Jr, Stankovic KM (1996) Medial efferent inhibition produces the largest equivalent attenuations at moderate to high sound levels in cat auditory-nerve fibers. J Acoust Soc Am 100:1680–1690PubMedGoogle Scholar
  40. Gulley RL, Reese TS (1977) Regional specialization of the hair cell plasmalemma in the organ of corti. Anat Rec 189:109–123PubMedGoogle Scholar
  41. Guth PS, Perin P, Norris CH, Valli P (1998) The vestibular hair cells: post-transductional signal processing. Prog Neurobiol 54:193–247PubMedGoogle Scholar
  42. Hackney CM, Mahendrasingam S, Penn A, Fettiplace R (2005) The concentrations of calcium buffering proteins in mammalian cochlear hair cells. J Neurosci 25:7867–7875PubMedGoogle Scholar
  43. Hallworth NE, Wilson CJ, Bevan MD (2003) Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J Neurosci 23:7525–7542PubMedGoogle Scholar
  44. He DZ, Jia S, Dallos P (2004a) Mechanoelectrical transduction of adult outer hair cells studied in a gerbil hemicochlea. Nature 429:766–770PubMedGoogle Scholar
  45. He DZ, Cheatham MA, Pearce M, Vetter DE (2004b) Mouse outer hair cells lacking the alpha9 ACh receptor are motile. Brain Res Dev Brain Res 148:19–25PubMedGoogle Scholar
  46. Hirokawa N (1978) The ultrastructure of the basilar papilla of the chick. J Comp Neurol 181:361–374PubMedGoogle Scholar
  47. Housley GD, Ashmore JF (1991) Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc R Soc Lond B Biol Sci 244:161–167Google Scholar
  48. Johnson SL, Adelman JP, Marcotti W (2007) Genetic deletion of SK2 channels in mouse inner hair cells prevents the developmental linearization in the Ca2+ dependence of exocytosis. J Physiol 583:631–646PubMedGoogle Scholar
  49. Jones MV, Westbrook GL (1996) The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci 19:96–101PubMedGoogle Scholar
  50. Kakehata S, Nakagawa T, Takasaka T, Akaike N (1993) Cellular mechanism of acetylcholine-induced response in dissociated outer hair cells of guinea-pig cochlea. J Physiol (Lond) 463:227–244Google Scholar
  51. Kandler K (2004) Activity-dependent organization of inhibitory circuits: lessons from the auditory system. Curr Opin Neurobiol 14:96–104PubMedGoogle Scholar
  52. Karlin A (2002) Emerging structure of the nicotinic acetylcholine receptors. Nat Rev Neurosci 3:102–114PubMedGoogle Scholar
  53. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133–1138PubMedGoogle Scholar
  54. Katz E, Verbitsky M, Rothlin CV, Vetter DE, Heinemann SF, Belen Elgoyhen A (2000) High calcium permeability and calcium block of the alpha9 nicotinic acetylcholine receptor. Hear Res 141:117–128PubMedGoogle Scholar
  55. Katz E, Elgoyhen AB, Gomez-Casati ME, Knipper M, Vetter DE, Fuchs PA, Glowatzki E (2004) Developmental regulation of nicotinic synapses on cochlear inner hair cells. J Neurosci 24:7814–7820PubMedGoogle Scholar
  56. Kiang NY, Moxon EC, Levine RA (1970) Auditory-nerve activity in cats with normal and abnormal cochleas. In: sensorineural hearing loss. Ciba Found Symp 241–273Google Scholar
  57. Kohler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, Adelman JP (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273:1709–1714PubMedGoogle Scholar
  58. Kong WJ, Cheng HM, van Cauwenberge P (2006) Expression of nicotinic acetylcholine receptor subunit alpha9 in type II vestibular hair cells of rats. Acta Pharmacol Sin 27:1509–1514PubMedGoogle Scholar
  59. Kong JH, Adelman JP, Fuchs PA (2008) Expression of the SK2 calcium-activated potassium channel is required for cholinergic function in mouse cochlear hair cells. J Physiol 586:5471–5485PubMedGoogle Scholar
  60. Kotak VC, Sanes DH (1995) Synaptically evoked prolonged depolarizations in the developing auditory system. J Neurophysiol 74:1611–1620PubMedGoogle Scholar
  61. Kros CJ, Ruppersberg JP, Rusch A (1998) Expression of a potassium current in inner hair cells during development of hearing in mice. Nature 394:281–284PubMedGoogle Scholar
  62. Labarca C, Schwarz J, Deshpande P, Schwarz S, Nowak M, Fonck C, Nashmi R, Kofuji P, Dang H, Shi W, Fidan M, Khakh B, Chen Z, Bowers B, Boulter J, Wehner J, Lester H (2001) Point mutant mice with hypersensitive alpha4 nicotinic receptors show dopaminergic deficits and increased anxiety. Proc Natl Acad Sci USA 98:2786–2791PubMedGoogle Scholar
  63. Leake PA, Hradek GT, Chair L, Snyder RL (2006) Neonatal deafness results in degraded topographic specificity of auditory nerve projections to the cochlear nucleus in cats. J Comp Neurol 497:13–31PubMedGoogle Scholar
  64. Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol 301:443–460PubMedGoogle Scholar
  65. Lioudyno M, Hiel H, Kong JH, Katz E, Waldman E, Parameshwaran-Iyer S, Glowatzki E, Fuchs PA (2004) A “synaptoplasmic cistern” mediates rapid inhibition of cochlear hair cells. J Neurosci 24:11160–11164PubMedGoogle Scholar
  66. Lu L, Zhang Q, Timofeyev V, Zhang Z, Young JN, Shin HS, Knowlton AA, Chiamvimonvat N (2007) Molecular coupling of a Ca2+-activated K+ channel to L-type Ca2+ channels via alpha-actinin2. Circ Res 100:112–120PubMedGoogle Scholar
  67. Maison SF, Luebke AE, Liberman MC, Zuo J (2002) Efferent protection from acoustic injury is mediated via alpha9 nicotinic acetylcholine receptors on outer hair cells. J Neurosci 22:10838–10846PubMedGoogle Scholar
  68. Maison SF, Adams JC, Liberman MC (2003) Olivocochlear innervation in the mouse: immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. J Comp Neurol 455:406–416PubMedGoogle Scholar
  69. Maison SF, Parker LL, Young L, Adelman JP, Zuo J, Liberman MC (2007) Overexpression of SK2 channels enhances efferent suppression of cochlear responses without enhancing noise resistance. J Neurophysiol 97:2930–2936PubMedGoogle Scholar
  70. Marcotti W, Johnson SL, Holley MC, Kros CJ (2003) Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. J Physiol 548:383–400PubMedGoogle Scholar
  71. Marcotti W, Johnson SL, Kros CJ (2004) A transiently expressed SK current sustains and modulates action potential activity in immature mouse inner hair cells. J Physiol 560:691–708PubMedGoogle Scholar
  72. Martin AR, Fuchs PA (1992) The dependence of calcium-activated potassium currents on membrane potential. Proc R Soc Lond B Biol Sci 250:71–76Google Scholar
  73. Matthews TM, Duncan RK, Zidanic M, Michael TH, Fuchs PA (2005) Cloning and characterization of SK2 channel from chicken short hair cells. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 191:491–503PubMedGoogle Scholar
  74. May BJ, Prosen CA, Weiss D, Vetter D (2002) Behavioral investigation of some possible effects of the central olivocochlear pathways in transgenic mice. Hear Res 171:142–157PubMedGoogle Scholar
  75. McNiven AI, Yuhas WA, Fuchs PA (1996) Ionic dependence and agonist preference of an acetylcholine receptor in hair cells. Audit Neurosci 2:63–77Google Scholar
  76. Millar NS (2008) RIC-3: a nicotinic acetylcholine receptor chaperone. Br J Pharmacol 153(suppl 1):S177–S183PubMedGoogle Scholar
  77. Morley BJ, Li HS, Hiel H, Drescher DG, Elgoyhen AB (1998) Identification of the subunits of the nicotinic cholinergic receptors in the rat cochlea using RT-PCR and in situ hybridization. Brain Res Mol Brain Res 53:78–87PubMedGoogle Scholar
  78. Murthy V, Maison SF, Taranda J, Haque N, Bond CT, Elgoyhen AB, Adelman JP, Liberman MC, Vetter DE (2009) SK2 channels are required for function and long-term survival of efferent synapses on mammalian outer hair cells. Mol Cell Neurosci 40:39–49PubMedGoogle Scholar
  79. Murugasu E, Russell IJ (1996) The effect of efferent stimulation on basilar membrane displacement in the basal turn of the guinea pig cochlea. J Neurosci 16:325–332PubMedGoogle Scholar
  80. Nenov AP, Norris C, Bobbin RP (1996) Acetylcholine responses in guinea pig outer hair cells. II Activation of a small conductance Ca2+-activated K+ channel. Hear Res 101:149–172PubMedGoogle Scholar
  81. Norris CH, Housley GD, Williams WH, Guth SL, Guth PS (1988) The acetylcholine receptors of the semicircular canal of the frog (Rana Pipiens). Hear Res 32:197–206PubMedGoogle Scholar
  82. Oatman LC (1976) Effects of visual attention on the intensity of auditory evoked potentials. Exp Neurol 51:41–53PubMedGoogle Scholar
  83. Oliver D, Klocker N, Schuck J, Baukrowitz T, Ruppersberg JP, Fakler B (2000) Gating of Ca2+-activated K+ channels controls fast inhibitory synaptic transmission at auditory outer hair cells. Neuron 26:595–601PubMedGoogle Scholar
  84. Orr-Urtreger A, Broide R, Kasten M, Dang H, Dani J, Beaudet A, Patrick J (2000) Mice homozygous for the L250T mutattion in the alpha7 nicotinic acetylcholine receptor show increased neuronal apoptosis and die within 1 day of birth. J Neurochem 74:2154–2166PubMedGoogle Scholar
  85. Plazas PV, Katz E, Gomez-Casati ME, Bouzat C, Elgoyhen AB (2005a) Stoichiometry of the alpha9alpha10 nicotinic cholinergic receptor. J Neurosci 25:10905–10912PubMedGoogle Scholar
  86. Plazas PV, De Rosa MJ, Gomez-Casati ME, Verbitsky M, Weisstaub N, Katz E, Bouzat C, Elgoyhen AB (2005b) Key roles of hydrophobic rings of TM2 in gating of the alpha9alpha10 nicotinic cholinergic receptor. Br J Pharmacol 145:963–974PubMedGoogle Scholar
  87. Rajan R (1988) Effect of electrical stimulation of the crossed olivocochlear bundle on temporary threshold shifts in auditory sensitivity. I. Dependence on electrical stimulation parameters. J Neurophysiol 60:549–568PubMedGoogle Scholar
  88. Rasmussen GL (1946) The olivary peduncle and other fiber projections of the superior olivary complex. J Comp Neurol 84:141–219PubMedGoogle Scholar
  89. Rothlin CV, Katz E, Verbitsky M, Elgoyhen AB (1999) The alpha9 nicotinic acetylcholine receptor shares pharmacological properties with type A gamma-aminobutyric acid, glycine, and type 3 serotonin receptors. Mol Pharmacol 55:248–254PubMedGoogle Scholar
  90. Rothlin CV, Lioudyno MI, Silbering AF, Plazas PV, Casati ME, Katz E, Guth PS, Elgoyhen AB (2003) Direct interaction of serotonin type 3 receptor ligands with recombinant and native alpha 9 alpha 10-containing nicotinic cholinergic receptors. Mol Pharmacol 63: 1067–1074PubMedGoogle Scholar
  91. Saito K (1980) Fine structure of the sensory epithelium of the guinea pig organ of Corti: afferent and efferent synapses of hair cells. J Ultrastruct Res 71:222–232PubMedGoogle Scholar
  92. Sewell W (1996) Neurotransmitters and synaptic transmission. In: Dallos P, Popper AN, Fay RR (eds) The cochlea. Springer, New York, pp 503–533Google Scholar
  93. Sgard F, Charpentier E, Bertrand S, Walker N, Caput D, Graham D, Bertrand D, Besnard F (2002) A novel human nicotinic receptor subunit, α10, that confers functionality to the α9-subunit. Mol Pharmacol 61:150–159PubMedGoogle Scholar
  94. Shigemoto T, Ohmori H (1990) Muscarinic agonists and ATP increase the intracellular Ca2+ concentration in chick cochlear hair cells. J Physiol (Lond) 420:127–148Google Scholar
  95. Shigemoto T, Ohmori H (1991) Muscarinic receptor hyperpolarizes cochlear hair cells of chick by activating Ca(2+)-activated K+ channels. J Physiol 442:669–690PubMedGoogle Scholar
  96. Simmons DD (2002) Development of the inner ear efferent system across vertebrate species. J Neurobiol 53:228–250PubMedGoogle Scholar
  97. Simmons DD, Moulding HD, Zee D (1996) Olivocochlear innervation of inner and outer hair cells during postnatal maturation: an immunocytochemical study. Brain Res Dev Brain Res 95:213–226PubMedGoogle Scholar
  98. Simmons DD, Bertolotto C, Kim J, Raji-Kubba J, Mansdorf N (1998) Choline acetyltransferase expression during a putative developmental waiting period. J Comp Neurol 397: 281–295PubMedGoogle Scholar
  99. Sridhar TS, Brown MC, Sewell WF (1997) Unique postsynaptic signaling at the hair cell efferent synapse permits calcium to evoke changes on two time scales. J Neurosci 17:428–437PubMedGoogle Scholar
  100. Sugai YJ, Sugitani M, Ooyama H (1992) Actions of cholinergic agonist and antagonists on the efferent synapse in frog sacculus. Hear Res 61:56–64PubMedGoogle Scholar
  101. Takahashi T, Momiyama A (1991) Single-channel currents underlying glycinergic inhibitory postsynaptic responses in spinal neurons. Neuron 7:965–969PubMedGoogle Scholar
  102. Taranda J, Maison SF, Ballestero JA, Katz E, Savino J, Vetter DE, Boulter J, Liberman MC, Fuchs PA, Elgoyhen AB (2009a) A point mutation in the hair cell nicotinic cholinergic receptor prolongs cochlear inhibition and enhances noise protection. PLoS Biol 7:e18PubMedGoogle Scholar
  103. Taranda J, Ballestero JA, Hiel H, Souza FS, Wedemeyer C, Gomez-Casati ME, Lipovsek M, Vetter DE, Fuchs PA, Katz E, Elgoyhen AB (2009b) 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 10:397–406PubMedGoogle Scholar
  104. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE (2007) The origin of spontaneous activity in the developing auditory system. Nature 450:50–55PubMedGoogle Scholar
  105. Verbitsky M, Rothlin C, Katz E, Elgoyhen AB (2000) Mixed nicotinic-muscarinic properties of the a9 nicotinic receptor. Neuropharmacology 39:2515–2524PubMedGoogle Scholar
  106. Vetter DE, Adams JC, Mugnani E (1991) Chemically distinct rat olivocochlear neurons. Synapse 7:21–43PubMedGoogle Scholar
  107. Vetter DE, Liberman MC, Mann J, Barhanin J, Boulter J, Brown MC, Saffiote-Kolman J, Heinemann SF, Elgoyhen AB (1999) Role of alpha9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 23:93–103PubMedGoogle Scholar
  108. Vetter DE, Katz E, Maison SF, Taranda J, Turcan S, Ballestero J, Liberman MC, Elgoyhen AB, Boulter J (2007) The alpha10 nicotinic acetylcholine receptor subunit is required for normal synaptic function and integrity of the olivocochlear system. Proc Natl Acad Sci USA 104:20594–20599PubMedGoogle Scholar
  109. Walsh E, McGee J, McFadden S, Liberman M (1998) Long-term effects of sectioning the olivocochlear bundle in neonatal cats. J Neurosci 18:3859–3869PubMedGoogle Scholar
  110. Warr WB (1975) Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J Comp Neurol 161:159–181PubMedGoogle Scholar
  111. Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Douglas W, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, New York, pp 410–448Google Scholar
  112. Warr WB, Guinan JJ Jr (1979) Efferent innervation of the organ of Corti: two separate systems. Brain Res 173:152–155PubMedGoogle Scholar
  113. Weisstaub N, Vetter DE, Elgoyhen AB, Katz E (2002) The alpha9alpha10 nicotinic acetylcholine receptor is permeable to and is modulated by divalent cations. Hear Res 167:122–135PubMedGoogle Scholar
  114. Wiederhold ML, Kiang NYS (1970) Effects of electrical stimulation of the crossed olivocochlear bundle on cat single auditory nerve fibres. J Acoust Soc Am 48:950–965PubMedGoogle Scholar
  115. Winslow RL, Sachs MB (1988) Single-tone intensity discrimination based on auditory-nerve rate responses in backgrounds of quiet, noise, and with stimulation of the crossed olivocochlear bundle. Hear Res 35:165–189PubMedGoogle Scholar
  116. Yoshida N, Shigemoto T, Sugai T, Ohmori H (1994) The role of inositol triphosphate on ACh-induced outward currents in bullfrog saccular hair cells. Brain Res 644:90–100PubMedGoogle Scholar
  117. Yuhas WA, Fuchs PA (1999) Apamin-sensitive, small-conductance, calcium-activated potassium channels mediate cholinergic inhibition of chick auditory hair cells. J Comp Physiol [A] 185:455–462Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Eleonora Katz
    • 1
  • Ana Belén Elgoyhen
  • Paul Albert Fuchs
  1. 1.Instituto de Investigaciones en Ingeniería Genética y Biología Molecular (Consejo Nacional de Investigaciones Científicas y Técnicas)Buenos AiresArgentina

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