The afferent signaling complex: Regulation of type I spiral ganglion neuron responses in the auditory periphery

Hearing Research

Volumn 336, Issue , 2016, Pages 1-16

  Reijntjes, Daniël O J ^a   Pyott, Sonja J ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Auditory neuropathy and synaptopathy; Cochlea; Inner hair cells; Ion channels and transporters; Lateral olivocochlear efferents; Neurotransmitter receptors; Postsynaptic density; Type I spiral ganglion neurons

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; AMPA RECEPTOR; CARRIER PROTEIN; DOPAMINE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL; ION CHANNEL; KAINIC ACID RECEPTOR; METABOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER RECEPTOR; VOLTAGE GATED POTASSIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

AMINO ACID TRANSPORT; AUDITORY NERVOUS SYSTEM; BRAIN STEM; CELL INTERACTION; CELL SPECIFICITY; CELLS BY BODY ANATOMY; COCHLEAR NERVE; DENDRITE; EFFERENT NERVE; GLUTAMATERGIC SYNAPSE; HUMAN; INNER HAIR CELL; INNERVATION; NERVE CELL MEMBRANE POTENTIAL; NERVE EXCITABILITY; NERVE FIBER; NERVE FUNCTION; NERVE GROWTH; NONHUMAN; POSTSYNAPTIC DENSITY; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; REGULATORY MECHANISM; REVIEW; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPIRAL GANGLION; ACTION POTENTIAL; ANIMAL; COCHLEA; GERBIL; GUINEA PIG; HEARING IMPAIRMENT; METABOLISM; MOUSE; NEWBORN; PHYSIOLOGY; RAT; SPINAL GANGLION; SYNAPSE; SYNAPTIC POTENTIAL;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; COCHLEA; DENDRITES; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; GANGLIA, SPINAL; GERBILLINAE; GUINEA PIGS; HAIR CELLS, AUDITORY, INNER; HEARING LOSS; HUMANS; MICE; NEURONS, AFFERENT; RATS; SIGNAL TRANSDUCTION; SPIRAL GANGLION; SYNAPSES; SYNAPTIC POTENTIALS;

EID: 84962883616     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2016.03.011     Document Type: Review

References (197)

1. Adamson C.L., Reid M.A., Davis R.L. Opposite actions of brain-derived neurotrophic factor and neurotrophin-3 on firing features and ion channel composition of murine spiral ganglion neurons. J. Neurosci. 2002, 22:1385-1396.
2. Adamson C.L., Reid M.A., Mo Z.L., Bowne-English J., Davis R.L. Firing features and potassium channel content of murine spiral ganglion neurons vary with cochlear location. J. Comp. Neurol. 2002, 447:331-350.
3. Albuquerque E.X., Pereira E.F., Alkondon M., Rogers S.W. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol. Rev. 2009, 89:73-120.
4. Anggono V., Huganir R.L. Regulation of AMPA receptor trafficking and synaptic plasticity. Curr. Opin. Neurobiol. 2012, 22:461-469.
5. Arnold T., Oestreicher E., Ehrenberger K., Felix D. GABA(A) receptor modulates the activity of inner hair cell afferents in guinea pig cochlea. Hear Res. 1998, 125:147-153.
6. Bakondi G., Por A., Kovacs I., Szucs G., Rusznak Z. Hyperpolarization-activated, cyclic nucleotide-gated, cation non-selective channel subunit expression pattern of guinea-pig spiral ganglion cells. Neuroscience 2009, 158:1469-1477.
7. Bao J., Lei D., Du Y., Ohlemiller K.K., Beaudet A.L., Role L.W. Requirement of nicotinic acetylcholine receptor subunit beta2 in the maintenance of spiral ganglion neurons during aging. J. Neurosci. 2005, 25:3041-3045.
8. Barbour B., Hausser M. Intersynaptic diffusion of neurotransmitter. Trends Neurosci. 1997, 20:377-384.
9. Barnard E.A., Skolnick P., Olsen R.W., Mohler H., Sieghart W., Biggio G., Braestrup C., Bateson A.N., Langer S.Z. International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function. Pharmacol. Rev. 1998, 50:291-313.
10. Bartlett T.E., Wang Y.T. The intersections of NMDAR-dependent synaptic plasticity and cell survival. Neuropharmacology 2013, 74:59-68.
11. Beaulieu J.M., Gainetdinov R.R. The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol. Rev. 2011, 63:182-217.
12. Beisel K.W., Rocha-Sanchez S.M., Morris K.A., Nie L., Feng F., Kachar B., Yamoah E.N., Fritzsch B. Differential expression of KCNQ4 in inner hair cells and sensory neurons is the basis of progressive high-frequency hearing loss. J. Neurosci. 2005, 25:9285-9293.
13. Benarroch E.E. GABAB receptors: structure, functions, and clinical implications. Neurology 2012, 78:578-584.
14. Benarroch E.E. HCN channels: function and clinical implications. Neurology 2013, 80:304-310.
15. Bettler B., Kaupmann K., Bowery N. GABAB receptors: drugs meet clones. Curr. Opin. Neurobiol. 1998, 8:345-350.
16. Borg E., Engstrom B., Linde G., Marklund K. Eighth nerve fiber firing features in normal-hearing rabbits. Hear Res. 1988, 36:191-201.
17. Braude J.P., Vijayakumar S., Baumgarner K., Laurine R., Jones T.A., Jones S.M., Pyott S.J. Deletion of Shank1 has minimal effects on the molecular composition and function of glutamatergic afferent postsynapses in the mouse inner ear. Hear Res. 2015, 321:52-64.
18. Brown M.C. Morphology of labeled afferent fibers in the guinea pig cochlea. J. Comp. Neurol. 1987, 260:591-604.
19. Catterall W.A., Goldin A.L., Waxman S.G. International union of pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol. Rev. 2005, 57:397-409.
20. Cerda O., Trimmer J.S. Analysis and functional implications of phosphorylation of neuronal voltage-gated potassium channels. Neurosci. Lett. 2010, 486:60-67.
21. Chapochnikov N.M., Takago H., Huang C.H., Pangrsic T., Khimich D., Neef J., Auge E., Gottfert F., Hell S.W., Wichmann C., Wolf F., Moser T. Uniquantal release through a dynamic fusion pore is a candidate mechanism of hair cell exocytosis. Neuron 2014, 83:1389-1403.
22. Chater T.E., Goda Y. The role of AMPA receptors in postsynaptic mechanisms of synaptic plasticity. Front. Cell Neurosci. 2014, 8:401.
23. Chen C. Hyperpolarization-activated current (Ih) in primary auditory neurons. Hear Res. 1997, 110:179-190.
24. Chen W.C., Xue H.Z., Hsu Y.L., Liu Q., Patel S., Davis R.L. Complex distribution patterns of voltage-gated calcium channel alpha-subunits in the spiral ganglion. Hear Res. 2011, 278:52-68.
25. Chen Z., Kujawa S.G., Sewell W.F. Auditory sensitivity regulation via rapid changes in expression of surface AMPA receptors. Nat. Neurosci. 2007, 10:1238-1240.
26. Chen Z., Kujawa S.G., Sewell W.F. Functional roles of high-affinity glutamate transporters in cochlear afferent synaptic transmission in the mouse. J. Neurophysiol. 2010, 103:2581-2586.
27. Chen Z., Peppi M., Kujawa S.G., Sewell W.F. Regulated expression of surface AMPA receptors reduces excitotoxicity in auditory neurons. J. Neurophysiol. 2009, 102:1152-1159.
28. Collingridge G.L., Olsen R.W., Peters J., Spedding M. A nomenclature for ligand-gated ion channels. Neuropharmacology 2009, 56:2-5.
29. Crozier R.A., Davis R.L. Unmasking of spiral ganglion neuron firing dynamics by membrane potential and neurotrophin-3. J. Neurosci. 2014, 34:9688-9702.
30. d'Aldin C., Puel J.L., Leducq R., Crambes O., Eybalin M., Pujol R. Effects of a dopaminergic agonist in the guinea pig cochlea. Hear Res. 1995, 90:202-211.
31. Darrow K.N., Maison S.F., Liberman M.C. Cochlear efferent feedback balances interaural sensitivity. Nat. Neurosci. 2006, 9:1474-1476.
32. Darrow K.N., Maison S.F., Liberman M.C. Selective removal of lateral olivocochlear efferents increases vulnerability to acute acoustic injury. J. Neurophysiol. 2007, 97:1775-1785.
33. Darrow K.N., Simons E.J., Dodds L., Liberman M.C. Dopaminergic innervation of the mouse inner ear: evidence for a separate cytochemical group of cochlear efferent fibers. J. Comp. Neurol. 2006, 498:403-414.
34. Davies C., Tingley D., Kachar B., Wenthold R.J., Petralia R.S. Distribution of members of the PSD-95 family of MAGUK proteins at the synaptic region of inner and outer hair cells of the guinea pig cochlea. Synapse 2001, 40:258-268.
35. Davis R.L., Liu Q. Complex primary afferents: what the distribution of electrophysiologically-relevant phenotypes within the spiral ganglion tells us about peripheral neural coding. Hear Res. 2011, 276:34-43.
36. Doleviczenyi Z., Halmos G., Repassy G., Vizi E.S., Zelles T., Lendvai B. Cochlear dopamine release is modulated by group II metabotropic glutamate receptors via GABAergic neurotransmission. Neurosci. Lett. 2005, 385:93-98.
37. Durand D., Pampillo M., Caruso C., Lasaga M. Role of metabotropic glutamate receptors in the control of neuroendocrine function. Neuropharmacology 2008, 55:577-583.
38. el Barbary A. Auditory nerve of the normal and jaundiced rat. II. Frequency selectivity and two-tone rate suppression. Hear Res. 1991, 54:91-104.
39. Eybalin M. Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol. Rev. 1993, 73:309-373.
40. Eybalin M., Caicedo A., Renard N., Ruel J., Puel J.L. Transient Ca2+-permeable AMPA receptors in postnatal rat primary auditory neurons. Eur. J. Neurosci. 2004, 20:2981-2989.
41. Felix D., Ehrenberger K. The efferent modulation of mammalian inner hair cell afferents. Hear Res. 1992, 64:1-5.
42. Friedman R.A., Van Laer L., Huentelman M.J., Sheth S.S., Van Eyken E., Corneveaux J.J., Tembe W.D., Halperin R.F., Thorburn A.Q., Thys S., Bonneux S., Fransen E., Huyghe J., Pyykko I., Cremers C.W., Kremer H., Dhooge I., Stephens D., Orzan E., Pfister M., Bille M., Parving A., Sorri M., Van de Heyning P.H., Makmura L., Ohmen J.D., Linthicum F.H., Fayad J.N., Pearson J.V., Craig D.W., Stephan D.A., Van Camp G. GRM7 variants confer susceptibility to age-related hearing impairment. Hum. Mol. Genet. 2009, 18:785-796.
43. Fryatt A.G., Vial C., Mulheran M., Gunthorpe M.J., Grubb B.D. Voltage-gated sodium channel expression in rat spiral ganglion neurons. Mol. Cell Neurosci. 2009, 42:399-407.
44. Fryatt A.G., Mulheran M., Egerton J., Gunthorpe M.J., Grubb B.D. Ototrauma induces sodium channel plasticity in auditory afferent neurons. Mol. Cell Neurosci. 2011, 48:51-61.
45. Fujikawa T., Petralia R.S., Fitzgerald T.S., Wang Y.X., Millis B., Morgado-Diaz J.A., Kitamura K., Kachar B. Localization of kainate receptors in inner and outer hair cell synapses. Hear Res. 2014, 314:20-32.
46. Furman A.C., Kujawa S.G., Liberman M.C. Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J. Neurophysiol 2013, 110:577-586.
47. Furness D.N., Lehre K.P. Immunocytochemical localization of a high-affinity glutamate-aspartate transporter, GLAST, in the rat and guinea-pig cochlea. Eur. J. Neurosci. 1997, 9:1961-1969.
48. Furness D.N., Lawton D.M. Comparative distribution of glutamate transporters and receptors in relation to afferent innervation density in the mammalian cochlea. J. Neurosci. 2003, 23:11296-11304.
49. Gaborjan A., Lendvai B., Vizi E.S. Neurochemical evidence of dopamine release by lateral olivocochlear efferents and its presynaptic modulation in guinea-pig cochlea. Neuroscience 1999, 90:131-138.
50. Garrett A.R., Robertson D., Sellick P.M., Mulders W.H. The actions of dopamine receptors in the guinea pig cochlea. Audiol. Neurootol. 2011, 16:145-157.
51. Gil-Loyzaga P.E. Neurotransmitters of the olivocochlear lateral efferent system: with an emphasis on dopamine. Acta Otolaryngol. 1995, 115:222-226.
52. Glowatzki E., Fuchs P.A. Transmitter release at the hair cell ribbon synapse. Nat. Neurosci. 2002, 5:147-154.
53. Glowatzki E., Grant L., Fuchs P. Hair cell afferent synapses. Curr. Opin. Neurobiol. 2008, 18:389-395.
54. Glowatzki E., Cheng N., Hiel H., Yi E., Tanaka K., Ellis-Davies G.C., Rothstein J.D., Bergles D.E. The glutamate-aspartate transporter GLAST mediates glutamate uptake at inner hair cell afferent synapses in the mammalian cochlea. J. Neurosci. 2006, 26:7659-7664.
55. Golding N.L., Oertel D. Synaptic integration in dendrites: exceptional need for speed. J. Physiol. 2012, 590:5563-5569.
56. Goutman J.D., Glowatzki E. Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16341-16346.
57. Grant L., Yi E., Glowatzki E. Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. J. Neurosci. 2010, 30:4210-4220.
58. Graydon C.W., Cho S., Diamond J.S., Kachar B., von Gersdorff H., Grimes W.N. Specialized postsynaptic morphology enhances neurotransmitter dilution and high-frequency signaling at an auditory synapse. J. Neurosci. 2014, 34:8358-8372.
59. Groff J.A., Liberman M.C. Modulation of cochlear afferent response by the lateral olivocochlear system: activation via electrical stimulation of the inferior colliculus. J. Neurophysiol. 2003, 90:3178-3200.
60. Gutman G.A., Chandy K.G., Adelman J.P., Aiyar J., Bayliss D.A., Clapham D.E., Covarriubias M., Desir G.V., Furuichi K., Ganetzky B., Garcia M.L., Grissmer S., Jan L.Y., Karschin A., Kim D., Kuperschmidt S., Kurachi Y., Lazdunski M., Lesage F., Lester H.A., McKinnon D., Nichols C.G., O'Kelly I., Robbins J., Robertson G.A., Rudy B., Sanguinetti M., Seino S., Stuehmer W., Tamkun M.M., Vandenberg C.A., Wei A., Wulff H., Wymore R.S., International Union of P. International union of pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels. Pharmacol. Rev. 2003, 55:583-586.
61. Hakuba N., Koga K., Shudou M., Watanabe F., Mitani A., Gyo K. Hearing loss and glutamate efflux in the perilymph following transient hindbrain ischemia in gerbils. J. Comp. Neurol. 2000, 418:217-226.
62. Hakuba N., Matsubara A., Hyodo J., Taniguchi M., Maetani T., Shimizu Y., Tsujiuchi Y., Shudou M., Gyo K. AMPA/kainate-type glutamate receptor antagonist reduces progressive inner hair cell loss after transient cochlear ischemia. Brain Res. 2003, 979:194-202.
63. Halmos G., Doleviczenyi Z., Repassy G., Kittel A., Vizi E.S., Lendvai B., Zelles T. D2 autoreceptor inhibition reveals oxygen-glucose deprivation-induced release of dopamine in guinea-pig cochlea. Neuroscience 2005, 132:801-809.
64. Hossain W.A., Antic S.D., Yang Y., Rasband M.N., Morest D.K. Where is the spike generator of the cochlear nerve? Voltage-gated sodium channels in the mouse cochlea. J. Neurosci. 2005, 25:6857-6868.
65. Huang L.C., Barclay M., Lee K., Peter S., Housley G.D., Thorne P.R., Montgomery J.M. Synaptic profiles during neurite extension, refinement and retraction in the developing cochlea. Neural Dev. 2012, 7:38.
66. Huganir R.L., Nicoll R.A. AMPARs and synaptic plasticity: the last 25 years. Neuron 2013, 80:704-717.
67. Inoue T., Matsubara A., Maruya S., Yamamoto Y., Namba A., Sasaki A., Shinkawa H. Localization of dopamine receptor subtypes in the rat spiral ganglion. Neurosci. Lett. 2006, 399:226-229.
68. Isaac J.T., Ashby M.C., McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007, 54:859-871.
69. Ito K., Dulon D. Nonselective cation conductance activated by muscarinic and purinergic receptors in rat spiral ganglion neurons. Am. J. Physiol. Cell Physiol. 2002, 282:C1121-C1135.
70. Jensen A.A., Fahlke C., Bjorn-Yoshimoto W.E., Bunch L. Excitatory amino acid transporters: recent insights into molecular mechanisms, novel modes of modulation and new therapeutic possibilities. Curr. Opin. Pharmacol. 2015, 20:116-123.
71. Jin Z., Liang G.H., Cooper E.C., Jarlebark L. Expression and localization of K channels KCNQ2 and KCNQ3 in the mammalian cochlea. Audiol. Neurootol. 2009, 14:98-105.
72. Johnston J., Forsythe I.D., Kopp-Scheinpflug C. Going native: voltage-gated potassium channels controlling neuronal excitability. J. Physiol. 2010, 588:3187-3200.
73. Johnston J., Griffin S.J., Baker C., Skrzypiec A., Chernova T., Forsythe I.D. Initial segment Kv2.2 channels mediate a slow delayed rectifier and maintain high frequency action potential firing in medial nucleus of the trapezoid body neurons. J. Physiol. 2008, 586:3493-3509.
74. Kaczmarek L.K., Bhattacharjee A., Desai R., Gan L., Song P., von Hehn C.A., Whim M.D., Yang B. Regulation of the timing of MNTB neurons by short-term and long-term modulation of potassium channels. Hear Res. 2005, 206:133-145.
75. Kaplan J.H. Biochemistry of Na,K-ATPase. Annu. Rev. Biochem. 2002, 71:511-535.
76. Khan K.M., Drescher M.J., Hatfield J.S., Khan A.M., Drescher D.G. Muscarinic receptor subtypes are differentially distributed in the rat cochlea. Neuroscience 2002, 111:291-302.
77. Kim Y.H., Holt J.R. Functional contributions of HCN channels in the primary auditory neurons of the mouse inner ear. J. Gen. Physiol. 2013, 142:207-223.
78. Kim K.X., Rutherford M.A. Maturation of NaV and KV Channel Topographies in the Auditory Nerve Spike Initiator before and after Developmental Onset of Hearing Function. J. Neurosci 2016, 36:2111-2118.
79. Knipper M., Kopschall I., Rohbock K., Kopke A.K., Bonk I., Zimmermann U., Zenner H. Transient expression of NMDA receptors during rearrangement of AMPA-receptor-expressing fibers in the developing inner ear. Cell Tissue Res. 1997, 287:23-41.
80. Kostandy B.B. The role of glutamate in neuronal ischemic injury: the role of spark in fire. Neurol. Sci. 2012, 33:223-237.
81. Kruse A.C., Kobilka B.K., Gautam D., Sexton P.M., Christopoulos A., Wess J. Muscarinic acetylcholine receptors: novel opportunities for drug development. Nat. Rev. Drug Discov. 2014, 13:549-560.
82. Kujawa S.G., Liberman M.C. Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear Res. 2015, 330(Pt B):191-199.
83. Kuriyama H., Jenkins O., Altschuler R.A. Immunocytochemical localization of AMPA selective glutamate receptor subunits in the rat cochlea. Hear Res. 1994, 80:233-240.
84. Le Prell C.G., Halsey K., Hughes L.F., Dolan D.F., Bledsoe S.C. Disruption of lateral olivocochlear neurons via a dopaminergic neurotoxin depresses sound-evoked auditory nerve activity. J. Assoc. Res. Otolaryngol. 2005, 6:48-62.
85. Le Prell C.G., Dolan D.F., Hughes L.F., Altschuler R.A., Shore S.E., Bledsoe S.C. Disruption of lateral olivocochlear neurons with a dopaminergic neurotoxin depresses spontaneous auditory nerve activity. Neurosci. Lett. 2014, 582:54-58.
86. Lei D., Gao X., Perez P., Ohlemiller K.K., Chen C.C., Campbell K.P., Hood A.Y., Bao J. Anti-epileptic drugs delay age-related loss of spiral ganglion neurons via T-type calcium channel. Hear Res. 2011, 278:106-112.
87. Lerma J. Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 2003, 4:481-495.
88. Lerma J., Marques J.M. Kainate receptors in health and disease. Neuron 2013, 80:292-311.
89. Li H.S., Niedzielski A.S., Beisel K.W., Hiel H., Wenthold R.J., Morley B.J. Identification of a glutamate/aspartate transporter in the rat cochlea. Hear Res. 1994, 78:235-242.
90. Liberman L.D., Liberman M.C. Dynamics of cochlear synaptopathy after acoustic overexposure. J. Assoc. Res. Otolaryngol. 2015, 16:205-219.
91. Liberman L.D., Wang H., Liberman M.C. Opposing gradients of ribbon size and AMPA receptor expression underlie sensitivity differences among cochlear-nerve/hair-cell synapses. J. Neurosci. 2011, 31:801-808.
92. Liberman M.C. Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am. 1978, 63:442-455.
93. Liberman M.C. Morphological differences among radial afferent fibers in the cat cochlea: an electron-microscopic study of serial sections. Hear Res. 1980, 3:45-63.
94. Liberman M.C. Efferent synapses in the inner hair cell area of the cat cochlea: an electron microscopic study of serial sections. Hear Res. 1980, 3:189-204.
95. Liberman M.C. Single-neuron labeling in the cat auditory nerve. Science 1982, 216:1239-1241.
96. Liberman M.C. Effects of chronic cochlear de-efferentation on auditory-nerve response. Hear Res. 1990, 49:209-223.
97. Liberman M.C., Dodds L.W., Pierce S. Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J. Comp. Neurol. 1990, 301:443-460.
98. Liberman M.C., Liberman L.D., Maison S.F. Efferent feedback slows cochlear aging. J. Neurosci. 2014, 34:4599-4607.
99. Lin X. Action potentials and underlying voltage-dependent currents studied in cultured spiral ganglion neurons of the postnatal gerbil. Hear Res. 1997, 108:157-179.
100. Lin X., Chen S., Chen P. Activation of metabotropic GABAB receptors inhibited glutamate responses in spiral ganglion neurons of mice. Neuroreport 2000, 11:957-961.
101. Liu Q., Manis P.B., Davis R.L. I h and HCN channels in murine spiral ganglion neurons: tonotopic variation, local heterogeneity, and kinetic model. J. Assoc. Res. Otolaryngol. 2014, 15:585-599.
102. Liu Q., Lee E., Davis R.L. Heterogeneous intrinsic excitability of murine spiral ganglion neurons is determined by Kv1 and HCN channels. Neuroscience 2014, 257:96-110.
103. Lopez I., Ishiyama G., Acuna D., Ishiyama A., Baloh R.W. Immunolocalization of voltage-gated calcium channel alpha1 subunits in the chinchilla cochlea. Cell Tissue Res. 2003, 313:177-186.
104. Lu Y. Metabotropic glutamate receptors in auditory processing. Neuroscience 2014, 274:429-445.
105. Luo L., Brumm D., Ryan A.F. Distribution of non-NMDA glutamate receptor mRNAs in the developing rat cochlea. J. Comp. Neurol. 1995, 361:372-382.
106. Lv P., Wei D., Yamoah E.N. Kv7-type channel currents in spiral ganglion neurons: involvement in sensorineural hearing loss. J. Biol. Chem. 2010, 285:34699-34707.
107. Lv P., Sihn C.R., Wang W., Shen H., Kim H.J., Rocha-Sanchez S.M., Yamoah E.N. Posthearing Ca(2+) currents and their roles in shaping the different modes of firing of spiral ganglion neurons. J. Neurosci. 2012, 32:16314-16330.
108. Lv P., Kim H.J., Lee J.H., Sihn C.R., Fathabad Gharaie S., Mousavi-Nik A., Wang W., Wang H.G., Gratton M.A., Doyle K.J., Zhang X.D., Chiamvimonvat N., Yamoah E.N. Genetic, cellular, and functional evidence for Ca2+ inflow through Cav1.2 and Cav1.3 channels in murine spiral ganglion neurons. J. Neurosci. 2014, 34:7383-7393.
109. Magee J.C., Johnston D. Plasticity of dendritic function. Curr. Opin. Neurobiol. 2005, 15:334-342.
110. Maison S.F., Adams J.C., Liberman M.C. Olivocochlear innervation in the mouse: immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization. J. Comp. Neurol. 2003, 455:406-416.
111. 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.
112. Maison S.F., Casanova E., Holstein G.R., Bettler B., Liberman M.C. Loss of GABAB receptors in cochlear neurons: threshold elevation suggests modulation of outer hair cell function by type II afferent fibers. J. Assoc. Res. Otolaryngol. 2009, 10:50-63.
113. Maison S.F., Liu X.P., Eatock R.A., Sibley D.R., Grandy D.K., Liberman M.C. Dopaminergic signaling in the cochlea: receptor expression patterns and deletion phenotypes. J. Neurosci. 2012, 32:344-355.
114. Maison S.F., Liu X.P., Vetter D.E., Eatock R.A., Nathanson N.M., Wess J., Liberman M.C. Muscarinic signaling in the cochlea: presynaptic and postsynaptic effects on efferent feedback and afferent excitability. J. Neurosci. 2010, 30:6751-6762.
115. Malgrange B., Rigo J.M., Lefebvre P.P., Coucke P., Goffin F., Xhauflaire G., Belachew S., Van de Water T.R., Moonen G. Diazepam-insensitive GABAA receptors on postnatal spiral ganglion neurones in culture. Neuroreport 1997, 8:591-596.
116. Malinow R., Malenka R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 2002, 25:103-126.
117. Matsubara A., Laake J.H., Davanger S., Usami S., Ottersen O.P. Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J. Neurosci. 1996, 16:4457-4467.
118. McLean W.J., Smith K.A., Glowatzki E., Pyott S.J. Distribution of the Na,K-ATPase alpha subunit in the rat spiral ganglion and organ of corti. J. Assoc. Res. Otolaryngol. 2009, 10:37-49.
119. Melyan Z., Wheal H.V., Lancaster B. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 2002, 34:107-114.
120. Melyan Z., Lancaster B., Wheal H.V. Metabotropic regulation of intrinsic excitability by synaptic activation of kainate receptors. J. Neurosci. 2004, 24:4530-4534.
121. Meredith A. Genetic methods for studying ion channel function in physiology and disease. Handbook of Ion Channles 2015, CRC Press. J. Zheng, M.C. Trudeau (Eds.).
122. Meyer A.C., Moser T. Structure and function of cochlear afferent innervation. Curr. Opin. Otolaryngol. Head. Neck Surg. 2010, 18:441-446.
123. Meyer A.C., Frank T., Khimich D., Hoch G., Riedel D., Chapochnikov N.M., Yarin Y.M., Harke B., Hell S.W., Egner A., Moser T. Tuning of synapse number, structure and function in the cochlea. Nat. Neurosci. 2009, 12:444-453.
124. Moore E.J., Hall D.B., Narahashi T. Sodium and potassium currents of type I spiral ganglion cells from rat. Acta Otolaryngol. 1996, 116:552-560.
125. Morley B.J., Li H.S., Hiel H., Drescher D.G., Elgoyhen A.B. 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. 1998, 53:78-87.
126. Morton-Jones R.T., Cannell M.B., Housley G.D. Ca2+ entry via AMPA-type glutamate receptors triggers Ca2+-induced Ca2+ release from ryanodine receptors in rat spiral ganglion neurons. Cell Calcium 2008, 43:356-366.
127. Moser T., Predoehl F., Starr A. Review of hair cell synapse defects in sensorineural hearing impairment. Otol. Neurotol. 2013, 34:995-1004.
128. Murashita H., Tabuchi K., Sakai S., Uemaetomari I., Tsuji S., Hara A. The effect of a GABAA agonist muscimol on acoustic injury of the mouse cochlea. Neurosci. Lett. 2007, 418:18-21.
129. Nakagawa T., Yamashita M., Hisashi K., Usami S.I., Kakazu Y., Shibata S., Nakashima T., Koike K., Kubo K., Komune S. GABA-induced response in spiral ganglion cells acutely isolated from guinea pig cochlea. Neurosci. Res. 2005, 53:396-403.
130. Nicoletti F., Bockaert J., Collingridge G.L., Conn P.J., Ferraguti F., Schoepp D.D., Wroblewski J.T., Pin J.P. Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology 2011, 60:1017-1041.
131. Niedzielski A.S., Wenthold R.J. Expression of AMPA, kainate, and NMDA receptor subunits in cochlear and vestibular ganglia. J. Neurosci. 1995, 15:2338-2353.
132. Niswender C.M., Conn P.J. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu. Rev. Pharmacol. Toxicol. 2010, 50:295-322.
133. Niu X., Canlon B. The signal transduction pathway for the dopamine D1 receptor in the guinea-pig cochlea. Neuroscience 2006, 137:981-990.
134. Niu X., Bogdanovic N., Canlon B. The distribution and the modulation of tyrosine hydroxylase immunoreactivity in the lateral olivocochlear system of the guinea-pig. Neuroscience 2004, 125:725-733.
135. Nouvian R., Eybalin M., Puel J.L. Cochlear efferents in developing adult and pathological conditions. Cell Tissue Res. 2015, 361:301-309.
136. Nouvian R., Beutner D., Parsons T.D., Moser T. Structure and function of the hair cell ribbon synapse. J. Membr. Biol. 2006, 209:153-165.
137. O'Brien J.E., Meisler M.H. Sodium channel SCN8A (Nav1.6): properties and de novo mutations in epileptic encephalopathy and intellectual disability. Front. Genet. 2013, 4:213.
138. Oak M.H., Yi E. Voltage-gated K(+) channels contributing to temporal precision at the inner hair cell-auditory afferent nerve fiber synapses in the mammalian cochlea. Arch. Pharm. Res. 2014, 37:821-833.
139. Oestreicher E., Arnold W., Ehrenberger K., Felix D. Dopamine regulates the glutamatergic inner hair cell activity in guinea pigs. Hear Res. 1997, 107:46-52.
140. Ohlemiller K.K., Echteler S.M. Functional correlates of characteristic frequency in single cochlear nerve fibers of the Mongolian gerbil. J. Comp. Physiol. A 1990, 167:329-338.
141. Okabe S. Molecular anatomy of the postsynaptic density. Mol. Cell Neurosci. 2007, 34:503-518.
142. Ottersen O.P., Takumi Y., Matsubara A., Landsend A.S., Laake J.H., Usami S. Molecular organization of a type of peripheral glutamate synapse: the afferent synapses of hair cells in the inner ear. Prog. Neurobiol. 1998, 54:127-148.
143. Peppi M., Landa M., Sewell W.F. Cochlear kainate receptors. J. Assoc. Res. Otolaryngol. 2012, 13:199-208.
144. Popa R., Anniko M., Arnold W., Oestreicher E. Alpha and beta subunits of acetylcholine receptors in the human inner ear. Acta Otolaryngol. 2000, 120:484-489.
145. Pujol R., Puel J.L. Excitotoxicity, synaptic repair, and functional recovery in the mammalian cochlea: a review of recent findings. Ann. N. Y. Acad. Sci. 1999, 884:249-254.
146. Rebillard G., Ruel J., Nouvian R., Saleh H., Pujol R., Dehnes Y., Raymond J., Puel J.L., Devau G. Glutamate transporters in the guinea-pig cochlea: partial mRNA sequences, cellular expression and functional implications. Eur. J. Neurosci. 2003, 17:83-92.
147. Reinhard L., Tidow H., Clausen M.J., Nissen P. Na(+), K (+)-ATPase as a docking station: protein-protein complexes of the Na(+), K (+)-ATPase. Cell Mol. Life Sci. 2013, 70:205-222.
148. Roehm P.C., Xu N., Woodson E.A., Green S.H., Hansen M.R. Membrane depolarization inhibits spiral ganglion neurite growth via activation of multiple types of voltage sensitive calcium channels and calpain. Mol. Cell Neurosci. 2008, 37:376-387.
149. Rome C., Luo D., Dulon D. Muscarinic receptor-mediated calcium signaling in spiral ganglion neurons of the mammalian cochlea. Brain Res. 1999, 846:196-203.
150. Ruel J., Chen C., Pujol R., Bobbin R.P., Puel J.L. AMPA-preferring glutamate receptors in cochlear physiology of adult guinea-pig. J. Physiol. 1999, 518(Pt 3):667-680.
151. Ruel J., Bobbin R.P., Vidal D., Pujol R., Puel J.L. The selective AMPA receptor antagonist GYKI 53784 blocks action potential generation and excitotoxicity in the guinea pig cochlea. Neuropharmacology 2000, 39:1959-1973.
152. Ruel J., Nouvian R., Gervais d'Aldin C., Pujol R., Eybalin M., Puel J.L. Dopamine inhibition of auditory nerve activity in the adult mammalian cochlea. Eur. J. Neurosci. 2001, 14:977-986.
153. Ruel J., Wang J., Dememes D., Gobaille S., Puel J.L., Rebillard G. Dopamine transporter is essential for the maintenance of spontaneous activity of auditory nerve neurones and their responsiveness to sound stimulation. J. Neurochem. 2006, 97:190-200.
154. Ruel J., Wang J., Rebillard G., Eybalin M., Lloyd R., Pujol R., Puel J.L. Physiology, pharmacology and plasticity at the inner hair cell synaptic complex. Hear Res. 2007, 227:19-27.
155. Ruel J., Chabbert C., Nouvian R., Bendris R., Eybalin M., Leger C.L., Bourien J., Mersel M., Puel J.L. Salicylate enables cochlear arachidonic-acid-sensitive NMDA receptor responses. J. Neurosci. 2008, 28:7313-7323.
156. Rusznak Z., Szucs G. Spiral ganglion neurones: an overview of morphology, firing behaviour, ionic channels and function. Pflugers Arch. 2009, 457:1303-1325.
157. Ryan A.F., Brumm D., Kraft M. Occurrence and distribution of non-NMDA glutamate receptor mRNAs in the cochlea. Neuroreport 1991, 2:643-646.
158. Sadeghi S.G., Pyott S.J., Yu Z., Glowatzki E. Glutamatergic signaling at the vestibular hair cell calyx synapse. J. Neurosci. 2014, 34:14536-14550.
159. Safieddine S., Eybalin M. Triple immunofluorescence evidence for the coexistence of acetylcholine, enkephalins and calcitonin gene-related peptide within efferent (olivocochlear) neurons of rats and Guinea-pigs. Eur. J. Neurosci. 1992, 4:981-992.
160. Safieddine S., El-Amraoui A., Petit C. The auditory hair cell ribbon synapse: from assembly to function. Annu. Rev. Neurosci. 2012, 35:509-528.
161. Safieddine S., Bartolami S., Wenthold R.J., Eybalin M. Pre- and postsynaptic M3 muscarinic receptor mRNAs in the rodent peripheral auditory system. Brain Res. Mol. Brain Res. 1996, 40:127-135.
162. Safieddine S., Eybalin M. Expression of mGluR1 alpha mRNA receptor in rat and guinea pig cochlear neurons. Neuroreport 1995, 7:193-196.
163. Sakai S., Tabuchi K., Murashita H., Hara A. Activation of the GABA(A) receptor ameliorates the cochlear excitotoxicity caused by kainic acid in the guinea pig. Tohoku J. Exp. Med. 2008, 215:279-285.
164. Sanchez J.T., Ghelani S., Otto-Meyer S. From development to disease: diverse functions of NMDA-type glutamate receptors in the lower auditory pathway. Neuroscience 2015, 285:248-259.
165. Santos-Sacchi J. Voltage-dependent ionic conductances of type I spiral ganglion cells from the guinea pig inner ear. J. Neurosci. 1993, 13:3599-3611.
166. Sattler R., Rothstein J.D. Regulation and dysregulation of glutamate transporters. Handb. Exp. Pharmacol. 2006, 277-303.
167. Schmiedt R.A. Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data. Hear Res. 1989, 42:23-35.
168. Shen H., Lin Z., Lei D., Han J., Ohlemiller K.K., Bao J. Old mice lacking high-affinity nicotine receptors resist acoustic trauma. Hear Res. 2011, 277:184-191.
169. Sheng M., Kim E. The Shank family of scaffold proteins. J. Cell Sci. 2000, 113(Pt 11):1851-1856.
170. Sheng M., Hoogenraad C.C. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu. Rev. Biochem. 2007, 76:823-847.
171. Sigel E., Steinmann M.E. Structure, function, and modulation of GABA(A) receptors. J. Biol. Chem. 2012, 287:40224-40231.
172. Simms B.A., Zamponi G.W. Neuronal voltage-gated calcium channels: structure, function, and dysfunction. Neuron 2014, 82:24-45.
173. Sobkowicz H.M., Rose J.E., Scott G.E., Slapnick S.M. Ribbon synapses in the developing intact and cultured organ of Corti in the mouse. J. Neurosci. 1982, 2:942-957.
174. Stolting G., Fischer M., Fahlke C. CLC channel function and dysfunction in health and disease. Front. Physiol. 2014, 5:378.
175. Sun W., Salvi R.J. Dopamine modulates sodium currents in cochlear spiral ganglion neurons. Neuroreport 2001, 12:803-807.
176. Taberner A.M., Liberman M.C. Response properties of single auditory nerve fibers in the mouse. J. Neurophysiol. 2005, 93:557-569.
177. Tang X., Zhu X., Ding B., Walton J.P., Frisina R.D., Su J. Age-related hearing loss: GABA, nicotinic acetylcholine and NMDA receptor expression changes in spiral ganglion neurons of the mouse. Neuroscience 2014, 259:184-193.
178. Traynelis S.F., Wollmuth L.P., McBain C.J., Menniti F.S., Vance K.M., Ogden K.K., Hansen K.B., Yuan H., Myers S.J., Dingledine R. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 2010, 62:405-496.
179. Tritsch N.X., Bergles D.E. Developmental regulation of spontaneous activity in the Mammalian cochlea. J. Neurosci. 2010, 30:1539-1550.
180. 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.
181. Tsuji J., Liberman M.C. Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J. Comp. Neurol. 1997, 381:188-202.
182. Usami S., Matsubara A., Fujita S., Shinkawa H., Hayashi M. NMDA (NMDAR1) and AMPA-type (GluR2/3) receptor subunits are expressed in the inner ear. Neuroreport 1995, 6:1161-1164.
183. Valdes-Baizabal C., Soto E., Vega R. Dopaminergic modulation of the voltage-gated sodium current in the cochlear afferent neurons of the rat. PLoS One 2015, 10:e0120808.
184. Wang L., Li J., Yu L., Li X. Regulation of dopamine D2 receptors in the guinea pig cochlea. Acta Otolaryngol. 2014, 134:738-743.
185. Wang W., Kim H.J., Lv P., Tempel B., Yamoah E.N. Association of the Kv1 family of K+ channels and their functional blueprint in the properties of auditory neurons as revealed by genetic and functional analyses. J. Neurophysiol. 2013, 110:1751-1764.
186. Wang W., Kim H.J., Lee J.H., Wong V., Sihn C.R., Lv P., Perez Flores M.C., Mousavi-Nik A., Doyle K.J., Xu Y., Yamoah E.N. Functional significance of K+ channel beta-subunit KCNE3 in auditory neurons. J. Biol. Chem. 2014, 289:16802-16813.
187. Warr W.B., Boche J.B., Neely S.T. Efferent innervation of the inner hair cell region: origins and terminations of two lateral olivocochlear systems. Hear Res. 1997, 108:89-111.
188. Wess J. Molecular biology of muscarinic acetylcholine receptors. Crit. Rev. Neurobiol. 1996, 10:69-99.
189. Winter I.M., Robertson D., Yates G.K. Diversity of characteristic frequency rate-intensity functions in guinea pig auditory nerve fibres. Hear Res. 1990, 45:191-202.
190. Yamamoto Y., Matsubara A., Ishii K., Makinae K., Sasaki A., Shinkawa H. Localization of gamma-aminobutyric acid A receptor subunits in the rat spiral ganglion and organ of Corti. Acta Otolaryngol. 2002, 122:709-714.
191. Yang K., Huang Z.W., Huang J., Zhang X.J., Xiao B.K. Expression of the neuron-specific potassium chloride cotransporter KCC2 in adult rat cochlear. Neurosci. Lett. 2008, 441:205-209.
192. Yi E., Roux I., Glowatzki E. Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J. Neurophysiol. 2010, 103:2532-2543.
193. Yin Y., Liberman L.D., Maison S.F., Liberman M.C. Olivocochlear innervation maintains the normal modiolar-pillar and habenular-cuticular gradients in cochlear synaptic morphology. J. Assoc. Res. Otolaryngol. 2014, 15:571-583.
194. Zhang X.D., Lee J.H., Lv P., Chen W.C., Kim H.J., Wei D., Wang W., Sihn C.R., Doyle K.J., Rock J.R., Chiamvimonvat N., Yamoah E.N. Etiology of distinct membrane excitability in pre- and posthearing auditory neurons relies on activity of Cl- channel TMEM16A. Proc. Natl. Acad. Sci. U. S. A. 2015, 112:2575-2580.
195. Zheng X.Y., Henderson D., McFadden S.L., Ding D.L., Salvi R.J. Auditory nerve fiber responses following chronic cochlear de-efferentation. J. Comp. Neurol. 1999, 406:72-86.
196. Zilberstein Y., Liberman M.C., Corfas G. Inner hair cells are not required for survival of spiral ganglion neurons in the adult cochlea. J. Neurosci. 2012, 32:405-410.
197. Zuccotti A., Lee S.C., Campanelli D., Singer W., Satheesh S.V., Patriarchi T., Geisler H.S., Kopschall I., Rohbock K., Nothwang H.G., Hu J., Hell J.W., Schimmang T., Ruttiger L., Knipper M. L-type CaV1.2 deletion in the cochlea but not in the brainstem reduces noise vulnerability: implication for CaV1.2-mediated control of cochlear BDNF expression. Front. Mol. Neurosci. 2013, 6:20.