Afferent Synaptic Mechanisms

The Senses: A Comprehensive Reference

Volumn 3, Issue , 2008, Pages 365-395

  Rutherford, M A ^a   Roberts, W M ^a  

^a UNIVERSITY OF OREGON   (United States)

Author keywords

Active zone; Auditory nerve fiber; Calcium; Calcium buffer; Exocytosis; First auditory synapse; Hair cell; Primary afferent synapse; Synaptic body; Synaptic ribbon; Synaptic vesicle cycle

Indexed keywords

EID: 81255141545     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012370880-9.00032-3     Document Type: Chapter

References (189)

1. Achanzar W.E., Ward S. A nematode gene required for sperm vesicle fusion. J. Cell Sci. 1997, 110:1073-1081.
2. Anderson D.J., Rose J.E., Hind J.E., Brugge J.F. Temporal position of discharges in single auditory nerve fibers within the cycle of a sine-wave stimulus: frequency and intensity effects. J. Acoust. Soc. Am. 1970, 49:1131-1139.
3. Armstrong C.E., Roberts W.M. Electrical properties of frog saccular hair cells: distortion by enzymatic dissociation. J. Neurosci. 1998, 18:2962-2973.
4. Armstrong C.E., Roberts W.M. Rapidly inactivating and non-inactivating calcium-activated potassium currents in frog saccular hair cells. J. Physiol. 2001, 536:49-65.
5. Art J.J., Fettiplace R. Variation of membrane properties in hair cells isolated from the turtle cochlea. J. Physiol. 1987, 385:207-242.
6. Art J.J., Wu Y.C., Fettiplace R. The calcium-activated potassium channels of turtle hair cells. J. Gen. Physiol. 1995, 105:49-72.
7. Balkema G.W. A synaptic antigen (B16) is localized in retinal synaptic ribbons. J. Comp. Neurol. 1991, 312:573-583.
8. Bodian D. Presynaptic bodies of auditory hair cells in old world monkeys. Anat. Rec. 1980, 197:379-386.
9. Bracewell R.N. The Fourier Transform and Its Applications 1999, McGraw-Hill Co.
10. Brandt A., Khimich D., Moser T. Few Cav1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J. Neurosci. 2005, 25:11577-11585.
11. Brandt A., Striessng J., Moser T. CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. J. Neurosci. 2003, 23:10832-10840.
12. Bunt A.H. Enzymatic digestion of synaptic ribbons in amphibian retinal photoreceptors. Brain Res. 1971, 25:571-577.
13. Burack M.A., Silverman M.A., Banker G. The role of selective transport in neuronal protein sorting. Neuron 2000, 26:465-474.
14. Buran B.N., Moser T., Gundelfinger E.D., Liberman M.C. Role of synaptic ribbons in auditory nerve responses in mice lacking the synaptic scaffolding protein Bassoon. Assoc. Res. Otolaryngol (ARO) Poster, 2006, Baltimore 2006.
15. Cheatham M.A., Dallos P. Longitudinal comparisons of IHC ac and dc receptor potentials recorded from the guinea pig cochlea. Hear Res. 1993, 68:107-114.
16. Chen X., Tomchick D.R., Kovrigin E., Arac D., Machius M., Sudhof T.C., Rizo J. Three-dimensional structure of the complexin/SNARE complex. Neuron 2002, 33:397-409.
17. Chimento T.C., Schreiner C.E. Adaptation and recovery from adaptation in single fiber responses of the cat auditory nerve. J. Acoust. Soc. Am. 1991, 90:263-273.
18. Chinnadurai G. CtBP family proteins: more than transcriptional corepressors. Bioessays 2002, 25:9-12.
19. Christensen-Dalsgaard J., Narins P.M. Sound and vibration sensitivity of VIIIth nerve fibers in the frogs Leptodactylus albilabris and Rana pipiens pipiens. J. Comp. Physiol. A 1993, 172:653-662.
20. Correia M.J. Filtering properties of hair cells. Ann. N. Y. Acad. Sci. 1992, 656:49-57.
21. Dallos P. Response characteristics of mammalian cochlear hair cells. J. Neurosci. 1985, 5:1591-1608.
22. Dambly-Chaudiere C., Sapede D., Soubiran F., Decorde K., Gompel N., Ghysen A. The lateral line of zebrafish: a model system for the analysis of morphogenesis and neural development in vertebrates. Biol. Cell 2003, 95:579-587.
23. 2+ signals. J. Physiol. 2003, 553:775-788.
24. de Boer E., Nuttall A.L. The mechanical waveform of the basilar membrane. III. Intensity effects. J. Acoust. Soc. Am. 2000, 107:1497-1507.
25. Delcomyn F. Foundations of Neurobiology 1998, W. H. Freeman.
26. Delgutte B. Representation of speech-like sounds in the discharge patterns of auditory-verve fibers. J. Acoust. Soc. Am. 1980, 68:843-857.
27. tom Dieck S., Altrock W.D., Kessels M.M., Qualmann B., Regus H., Brauner D., Fejtova A., Bracko O., Gundelfinger E.D., Brandstatter J.H. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and Ribeye is essential for the assembly of the ribbon complex. J. Cell Biol. 2005, 168:825-836.
28. Dobrunz L.E., Stevens C.F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 1997, 18:995-1008.
29. Edmonds B.W., Gregory F.D., Schweizer F.E. Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells. J. Physiol. 2004, 560:439-450.
30. Edmonds B., Reyes R., Schwaller B., Roberts W.M. Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat. Neurosci. 2000, 3:786-790.
31. Eisen M.D., Spassova M., Parsons T.D. Large releasable pool of synaptic vesicles in chick cochlear hair cells. J. Neurophysiol. 2004, 91:2422-2428.
32. Fettiplace R., Fuchs P.A. Mechanisms of hair cell tuning. Annu. Rev. Physiol. 1999, 61:809-834.
33. Fuchs P.A. Time and intensity coding at the hair cell's ribbon synapse. J. Physiol. 2005, 566:7-12.
34. Fuchs P.A., Glowatzki E., Moser T. The afferent synapse of cochlear hair cells. Curr. Opin. Neurobiol. 2003, 13:452-458.
35. 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.
36. 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.
37. Furukawa T., Matsuura S. Adaptive rundown of excitatory post-synaptic potentials at synapses between hair cells and eighth nerve fibers in the goldfish. J. Physiol. 1978, 276:193-209.
38. Furukawa T., Hayashida Y., Matsuura S. Quantal analysis of the size of excitatory post-synaptic potentials at synapses between hair cells and afferent nerve fibers in the goldfish. J. Physiol. 1978, 276:211-226.
39. Furukawa T., Kuno M., Matsuura S. Quantal analysis of a decremental response at hair cell-afferent fibre synapses in the goldfish sacculus. J. Physiol. 1982, 322:181-195.
40. Gaumond R.P., Kim D.O., Molnar C.E. Response of cochlear nerve fibers to brief acoustic stimuli: role of discharge-history effects. J. Acoust. Soc. Am. 1983, 74:1392-1398.
41. von Gersdorff H., Matthews G. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J. Neurosci. 1997, 17:1919-1927.
42. von Gersdorff H., Sakaba T., Berglund K., Tachibana M. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 1998, 21:1177-1188.
43. Giannessi F., Ruffoli R. Fine structure of the afferent synapses in the paratympanic organ of the chicken, with special reference to the synaptic bodies. Ann. Anat. 1996, 178:127-131.
44. Gitler D., Takagishi Y., Feng J., Ren Y., Rodriguiz R.M., Wetsel W.C., Greengard P., Augustine G.J. Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J. Neurosci. 2004, 24:11368-11380.
45. Gleisner L., Flock A., Wersall J. The ultrastructure of the afferent synapse on hair cells in the frog labyrinth. Acta Otolaryngol. 1973, 76:199-207.
46. Glowatzki E., Fuchs P.A. Transmitter release at the hair cell ribbon synapse. Nat. Neurosci. 2002, 5:147-154.
47. Goldberg J.M. Theoretical analysis of intercellular communication between the vestibular type I hair cell and its calyx ending. J. Neurophysiol. 1996, 76:1942-1957.
48. Gray E.G., Pease H.L. On understanding the origins of the retinal receptor synapses. Brain Res. 1971, 35:1-15.
49. Griesinger C.B., Richards C.D., Ashmore J.F. Fast vesicle replenishment allows indefatigable signaling at the first auditory synapse. Nature 2005, 435:212-215.
50. Hackney C.M., Mahendrasingam S., Penn A., Fettiplace R. The concentrations of calcium buffering proteins in mammalian cochlear hair cells. J. Neurosci. 2005, 25:7867-7886.
51. Hakuba N., Koga K., Gyo K., Usami S., Tanaka K. Exacerbation of noise-induced hearing loss in mice lacking the glutamate transporter GLAST. J. Neurosci. 2000, 20:8750-8753.
52. Hama K., Saito K. Fine structure of the afferent synapse of the hair cells in the saccular macula of the goldfish, with special reference to the anastomosing tubules. J. Neurocytol. 1977, 6:361-373.
53. Harris D.M., Dallos P. Forward masking of auditory nerve fiber responses. J. Neurophysiol. 1979, 42:1083-1107.
54. Hashimoto S., Kimura R.S., Takasaka T. Computer-aided 3-dimensional reconstruction of the inner hair-cells and their nerve-endings in the guinea-pig. Acta Otolaryngol. 1990, 109:228-234.
55. Heidelberger R., Sterling P., Matthews G. Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. J. Neurophysiol. 2002, 88:98-106.
56. Heil P., Neubauer H. Temporal integration of sound pressure determines thresholds of auditory nerve fibers. J. Neurosci. 2001, 21:7404-7415.
57. Heil P., Neubauer H. A unifying basis of auditory thresholds based on temporal summation. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:6151-6156.
58. 2+ buffer in hair cells. JARO 2002, 3:488-498.
59. Hilfiker S., Pieribone V.A., Czernik A.J., Kao H.T., Augustine G.J., Greengard P. Synapsins as regulators of neurotransmitter release. Phil. Trans. R Soc. Lond. B 1999, 354:269-279.
60. Hille B. Ionic Channels of Excitable Membranes 2001, Sinauer Associates.
61. Hirokawa N., Sobue K., Kanda K., Harada A., Yorifuji H. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J. Cell Biol. 1989, 108:111-126.
62. Holt M., Cooke A., Neef A., Lagnado L. High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr. Biol. 2004, 14:173-183.
63. Holt J.C., Xue J.T., Brichta A.M., Goldberg J.M. Transmission between type II hair cells and bouton afferents in the turtle posterior crista. J. Neurophysiol. 2006, 95:428-452.
64. Holton T., Weiss T.F. Receptor potentials of lizard cochlear hair cells with free-standing stereocilia in response to tones. J. Physiol. 1983, 345:205-240.
65. Hossain W.A., Antic S.D., Yang Y., Rasband M.N., Morest D.K. Where is the spike generator of the cochlear nerve?. J. Neurosci. 2005, 25:6857-6868.
66. Indresano A.A., Frank J.E., Middleton P., Jaramillo F. Mechanical noise enhances signal transmission in the bullfrog sacculus. JARO 2004, 4:363-370.
67. + channels at fluorescently labeled presynaptic active zones of hair cells. Proc. Natl. Acad. Sci. U. S. A. 1994, 91:7578-7582.
68. Jacobs R.A., Hudspeth A.J. Ultrastructural correlates of mechanoelectrical transduction in hair-cells of the bullfrogs internal ear. Cold Spring Harb. Symp. Quant. Biol. 1990, 55:547-561.
69. Javel E., Mott J.B. Physiological and psychophysical correlates of temporal processes in hearing. Hear Res. 1988, 34:275-294.
70. Jeffress L.A. Mathematical and electrical models of auditory detection. J. Acoust. Soc. Am. 1968, 44:187-203.
71. Johnson D.H. The relationship between spike rate and synchrony in responses of auditory-nerve fibers to single tones. J. Acoust. Soc. Am. 1980, 68:1115-1122.
72. Johnson D.H., Kiang N.Y.S. Analysis of discharges recorded simultaneously from pairs of auditory nerve fibers. Biophys. J. 1976, 16:719-734.
73. 2+ dependence of exocytosis during development of mouse inner hair cells. J. Physiol. 2005, 563:177-191.
74. + channel spliced variants in the tonotopic organization of the turtle cochlea. J. Physiol. 1999, 518:653-665.
75. Kandel E.R., Schwartz J.H., Jessell T.M. Principles of Neural Science 2000, McGraw-Hill.
76. Keen E.C., Hudspeth A.J. Transfer characteristics of the hair cell's afferent synapse. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5537-5542.
77. Khimich D., Nouvian R., Pujol R., tom Dieck S., Egner A., Gundelfinger E.D., Moser T. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 2005, 434:889-894.
78. Kiang N.Y.S., Rho J.M., Northrop C.C., Liberman M.C., Ryugo D.K. Hair-cell innervation by spiral ganglion cells in adult cats. Science 1982, 217:175-177.
79. Kiang N.Y.S., Watanabe T., Thomas E.C., Clark L.F. Discharge Pattern of Single Fibers in the Cat's Auditory Nerve 1965, MIT Press.
80. King T.S., Dougherty W.J. Effect of denervation on "synaptic" ribbon population in the rat pineal gland. J. Neurocytol. 1982, 11:19-28.
81. Knudsen E.I., Konishi M. A neural map of auditory space in the owl. Science 1978, 200:795-797.
82. 2+ channels activating at negative voltages. J. Biol. Chem. 2001, 276:22100-22106.
83. Koyama H., Lewis E.R., Leverenz E.L., Baird R.A. Acute seismic sensitivity in the bullfrog ear. Brain Res. 1982, 250:168-172.
84. von Kriegstein K., Schmitz F., Link E., Sudhof T.C. Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur. J. Neurosci. 1999, 11:1335-1348.
85. Krstic R. Ultracytochemistry of the synaptic ribbons in the rat pineal organ. Cell Tissue Res. 1976, 166:135-143.
86. Lenzi D., von Gersdorff H. Structure suggests function: the case for synaptic ribbons as exocytotic nanomachines. Bioessays 2001, 23:831-840.
87. Lenzi D., Crum J., Ellisman M.H., Roberts W.M. Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 2002, 36:649-659.
88. Lenzi D., Runyeon J.W., Crum J., Ellisman M.H., Roberts W.M. Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J. Neurosci. 1999, 19:119-132.
89. Lewis E.R., Narins P.M. Do frogs communicate with seismic signals?. Science 1985, 227:187-189.
90. Lewis R.S., Hudspeth A.J. Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature 1983, 304:538-541.
91. Lewis E.R., Baird R.A., Leverenz E.L., Koyama H. Inner ear: dye injection reveals peripheral origins of specific sensitivities. Science 1982, 215:1641-1643.
92. 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.
93. Liberman M.C. Single-neuron labeling of the cat auditory nerve. Science 1982, 216:1239-1241.
94. Liberman M.C., Kiang N.Y.S. Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. Acta Otolaryngol. Suppl. 1978, 358:1-63.
95. 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.
96. Lindau M., Neher E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch. 1988, 411:137-146.
97. 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.
98. Manley G.A., Köppl C., Yates G.K. Activity of primary auditory neurons in the cochlear ganglion of the emu Dromaius novaehollandiae: spontaneous discharge, frequency tuning, and phase locking. J. Acoust. Soc. Am. 1997, 101:1560-1573.
99. Martinez-Dunst C., Michaels R.L., Fuchs P.A. Release sites and calcium channels in hair cells of the chick's cochlea. J. Neurosci. 1997, 17:9133-9144.
100. 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.
101. McMahon H.T., Missler M., Li C., Sudhof T.C. Complexins: cytosolic proteins that regulate SNAP receptor function. Cell 1995, 83:111-119.
102. Merchan-Perez A., Liberman M.C. Ultrastructural differences among afferent synapses on cochlear hair cells: correlations with spontaneous discharge rate. J. Comp. Neurol. 1996, 371:208-221.
103. Miller M.R., Beck J. Heterotopic synaptic bodies in the auditory hair cells of adult lizards. Anat. Rec. 1987, 218:338-344.
104. Morgans C.W. Localization of the α1F calcium channel subunit in the rat retina. Invest. Ophthalmol. Vis. Sci. 2001, 42:2414-2418.
105. Morgans C.W., Brandstatter J.H., Kellerman J., Betz H., Wassle H. SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. J. Neurosci. 1996, 16:6713-6721.
106. Moser T., Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:883-888.
107. Moser T., Brandt A., Lysakowski A. Hair cell ribbon synapses. Cell Tissue Res. 2006, 326:347-359.
108. Moser T., Neef A., Khimich D. Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J. Physiol. 2006, 576:55-62.
109. Mountain D.C., Hubbard A.E. Computational Analysis of Hair Cell and Auditory Nerve Processes. Auditory Computation 1996, 121. Springer. H.L. Hawkins, T.A. McMullen, A.N. Popper, R.R. Fay (Eds.).
110. Muresan V., Lyass A., Schnapp B.J. The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. J. Neurosci. 1999, 19:1027-1037.
111. Nakagawa T., Oghalai J.S., Saggau P., Rabbitt R.D., Brownell W.E. Photometric recording of transmembrane potential in outer hair cells. J. Neural. Eng. 2006, 3:79-86.
112. Neher E., Augustine G.J. Calcium gradients and uffers in bovine chromaffin cells. J. Physiol. 1992, 450:273-301.
113. Nguyen T.H., Balkema G.W. Antigenic epitopes of the photoreceptor synaptic ribbon. J. Comp. Neurol. 1999, 413:209-218.
114. Nibu Y., Zhang H., Bajor E., Barolo S., Small S., Levine M. dCtBP mediates transcriptional repression by Knirps, Krueppel and Snail in the Drosophila embryo. EMBO J. 1998, 17:7009-7020.
115. Nicholls J.G., Martin A.R., Wallace B.G., Fuchs P.A. From Neuron to Brain 2001, Sinauer Associates.
116. Nouvian R., Beutner D., Parsons T.D., Moser T. Structure and function of the hair cell ribbon synapse. J. Memb. Biol. 2006, 209:1-13.
117. Osborne M.P., Thornhill R.A. The effect of monoamine depleting drugs upon the synaptic bars in the inner ear of the bullfrog. Z. Zellforsch. Mikrosk. Anat. 1972, 127:347-355.
118. Pabst S., Hazzard J.W., Antonin W., Sudhof T.C., Jahn R., Rizo J., Fasshauer D. Selective interaction of complexin with the neuronal SNARE complex. J. Biol. Chem. 2000, 275:19808-19818.
119. Palmer A.R., Russell I.J. Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells. Hear Res. 1986, 24:1-15.
120. Parsons T.D., Sterling P. Synaptic ribbon: conveyor belt or safety belt?. Neuron 2003, 37:379-382.
121. Parsons T.D., Lenzi D., Almers W., Roberts W.M. Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 1994, 13:875-883.
122. Plack C.J., Oxenham A.J., Drga V. Masking by inaudible sounds and the linearity of temporal summation. J. Neurosci. 2006, 26:8767-8773.
123. Poortinga G., Watanabe M., Parkhurst S.M. Drosophila CtBP: a hairy-interacting protein required for embryonic segmentation and hairy-mediated transcriptional repression. EMBO J. 1998, 17:2067-2078.
124. Pyle J.L., Kavalali E.T., Piedras-Renteria E.S., Tsien R.W. Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 2000, 28:221-231.
125. Raphael Y., Altschuler R.A. Structure and innervation of the cochlea. Brain Res. Bull. 2003, 60:397-422.
126. 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.
127. Rea R., Li J., Dharia A., Levitan E.S., Sterling P., Kramer R.H. Streamlined synaptic vesicle cycle in cone photoreceptor terminals. Neuron 2004, 41:755-766.
128. 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.
129. 2+-dependent neurotransmitter release. Cell 2001, 104:71-81.
130. Reim K., Wegmeyer H., Brandstatter J.H., Xue M., Rosenmund C., Dresbach T., Hofmann K., Brose N. Structurally and functionally unique complexins at retinal ribbon synapses. J. Cell Biol. 2006, 169:669-680.
131. Relkin E.M., Doucet J.R. Recovery from prior stimulation. I. Relationship to spontaneous firing rates of primary auditory neurons. Hear Res. 1991, 55:215-222.
132. Ricci A.J., Gray-Keller M., Fettiplace R. Tonotopic variations of calcium signalling in turtle auditory hair cells. J. Physiol. 2000, 524:423-436.
133. Rizzoli S.O., Betz W.J. Synaptic vesicle pools. Nat. Rev. Neurosci. 2005, 6:57-69.
134. Roberts W.M. Spatial calcium buffering in saccular hair cells. Nature 1993, 363:74-76.
135. Roberts W.M. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J. Neurosci. 1994, 14:3246-3262.
136. Roberts W.M., Jacobs R.A., Hudspeth A.J. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zone of hair cells. J. Neurosci. 1990, 10:3664-3684.
137. Robertson D. Horseradish peroxidase injection of physiologically characterized afferent and efferent neurons in the guinea pig spiral ganglion. Hear Res. 1984, 15:113-121.
138. Robertson D., Paki B. A role for purinergic receptors at the inner hair cell-afferent synapse?. Audiol. Neurootol. 2002, 7:62-67.
139. 2+ currents in bullfrog hair cells reveals two distinct channel subtypes. J. Physiol. 2001, 534:669-689.
140. 2+ channels in hair cells. Biophys. J. 2003, 84:3457-3469.
141. Rosahl T., Spillane D., Missler M., Herz J., Selig D., Wolff J.R., Hammer R.E., Malenka R.C., Sudhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 1995, 375:488-493.
142. Rose J.E., Brugge J.F., Anderson D.J., Hind J.E. Phase-locked response to low-frequency tones in single auditory nerve fibers of the squirrel monkey. J. Neurophysiol. 1967, 30:769-793.
143. Rose J.E., Hind J.E., Anderson D.J., Brugge J.F. Some effects of stimulus intensity on response of auditory-nerve fibers in the squirrel monkey. J. Neurophysiol. 1971, 34:685-699.
144. Rosenmund C., Rettig J., Brose N. Molecular mechanisms of active zone function. Curr. Opin. Neurobiol. 2003, 13:509-519.
145. 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.
146. Russell I.J., Sellick P.M. Intracellular studies of hair cells in the mammalian cochlea. J. Physiol. 1978, 284:261-290.
147. Rutherford M.A., Roberts W.M. Frequency selectivity of exocytosis in frog saccular hair cells. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2898-2903.
148. Safieddine S., Wenthold R.J. SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle- and synaptic membrane-associated proteins. Eur. J. Neurosci. 1999, 11:803-812.
149. 2+ on synaptic morphology of fish cone photoreceptors. Brain Res. 1991, 546:341-344.
150. Schmitz F., Konigstorfer A., Sudhof T.C. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 2000, 28:857-872.
151. Schnee M.E., Ricci A.J. Biophysical and pharmacological characterization of voltage-gated calcium currents in turtle auditory hair cells. J. Physiol. 2003, 549:697-717.
152. Schnee M.E., Lawton D.M., Furness D.N., Benke T.A., Ricci A.J. Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 2005, 47:243-254.
153. Schneggenburger R., Neher E. Presynaptic calcium and control of vesicle fusion. Curr. Opin. Neurobiol. 2005, 15:266-274.
154. Sewell W.F. The relation between the endocochlear potential and spontaneous activity in auditory nerve fibres of the cat. J. Physiol. 1984, 347:685-696.
155. Siegel J.H. Spontaneous synaptic potentials from afferent terminals in the guinea pig cochlea. Hear Res. 1992, 59:85-92.
156. Siegel J.H., Brownell W.E. Synaptic bodies in outer hair cells of the chinchilla organ of Corti. Brain Res. 1981, 220:188-193.
157. Siegel J.H., Brownell W.E. Synaptic and golgi membrane recycling in cochlear hair cells. J. Neurocytol. 1986, 15:311-328.
158. Singer J.H., Lassova L., Vardi N., Diamond J.S. Coordinated multivesicular release at a mammalian ribbon synapse. Nat. Neurosci. 2004, 7:826-833.
159. Sjöstrand F.S. Ultrastructure of retinal rod synapses of the guinea pig eye as revealed by three-dimensional reconstructions from serial sections. J. Ultrastruct. Res. 1958, 5:13-17.
160. Slepecky N.B., Galsky M.D., Swartzentruber-Martin H., Savage J. Study of afferent nerve terminals and fibers in the gerbil cochlea: distribution by size. Hear Res. 2000, 144:124-134.
161. Smith R.L. Short-term adaptation in single auditory nerve fibers: some poststimulatory effects. J. Neurophysiol. 1977, 40:1098-1111.
162. Smith C.A., Sjostrand F.S. Structure of the nerve endings on the external hair cells of the guinea pig cochlea as studied by serial sections. J. Ultrastruct. Res. 1961, 5:523556.
163. Smotherman M.S., Narins P.M. Hair cells, hearing and hopping: a field guide to hair cell physiology in the frog. J. Exp. Biol. 2000, 203:2237-2246.
164. Sneary M.G. Auditory receptor of the red-eared turtle: II. Afferent and efferent synapses and innervation patterns. J. Comp. Neurol. 1988, 276:588-606.
165. Sobkowicz H.M., August B.K., Slapnick S.M. Synaptic arrangements between inner hair cells and tunnel fibers in the mouse cochlea. Synapse 2004, 52:299-315.
166. Sobkowicz H.M., Rose J.E., Scott G.L., Levenick C.V. Distribution of synaptic ribbons in the developing organ of Corti. J. Neurocytol. 1986, 15:693-714.
167. Sobkowicz H.M., Slapnick S.M., August B.K. Reciprocal synapses between inner hair cell spines and afferent dendrites in the organ of corti of the mouse. Synapse 2003, 50:53-66.
168. Spassova M.A., Avissar M., Furman A.C., Crumling M.A., Saunders J.C., Parsons T.D. Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse. JARO 2004, 5:376390.
169. Spoendlin H. Innervation patterns in the organ of Corti of the cat. Acta Otolaryngol. 1969, 67:239-254.
170. Spoendlin H. Anatomy of cochlear innervation. Am. J. Otolaryngol. 1985, 6:453-467.
171. Sterling P., Matthews G. Structure and function of ribbon synapses. Trends Neurosci. 2005, 28:20-29.
172. Stern M.D. Buffering of calcium in the vicinity of a channel pore. Cell Calcium 1992, 13:183-192.
173. Stevens C.F., Williams J.H. "Kiss and run" exocytosis at hippocampal synapses. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:12828-12833.
174. Sudhof T.C. The synaptic vesicle cycle revisited. Neuron 2000, 28:317-320.
175. Sudhof T.C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 2004, 27:509-547.
176. Sumner C.J., Lopez-Poveda E.A., O'Mard L.P., Meddis R. A revised model of the inner-hair cell and auditory nerve complex. J. Acoust. Soc. Am. 2002, 111:2178-2188.
177. Tsuji J., Liberman M.C. Intracellular labeling of auditory nerve fibers in the guinea pig: central and peripheral projections. J. Comp. Neurol. 1997, 381:188-202.
178. Usukura J., Yamada E. Ultrastructure of the synaptic ribbons in photoreceptor cells of Rana catesbeiana revealed by freeze-etching and freeze-substitution. Cell Tissue Res. 1987, 247:483-488.
179. Wagner H.-J. Cell types and connectivity patterns in mosaic retinas. Adv. Anat. Embryol. Cell Biol. 1978, 55:1-81.
180. Wagner H.-J. Presynaptic bodies ("ribbons"): from ultrastructural observations to molecular perspectives. Cell Tissue Res. 1997, 287:435-446.
181. Wan L., Almers W., Chen W. Two ribeye genes in teleosts: the role of Ribeye in ribbon formation and bipolar cell development. J. Neurosci. 2005, 25:941-994.
182. Xu W., Lipscombe D. Neuronal Cav1.3α1 L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J. Neurosci. 2001, 21:5944-5951.
183. Yamazaki H., Nakata T., Okada Y., Hirokawa N. KIF3A/B: a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. J. Cell Biol. 1995, 130:1387-1399.
184. Yasunaga S., Grati M., Chardenoux S., Smith T.N., Friedman T.B., Lalwani A.K., Wilcox E.R., Petit C. OTOF encodes multiple long and short isoforms: genetic evidence that the long ones underlie recessive deafness DFNB9. Am. J. Hum. Genet. 2000, 67:591-600.
185. Yasunaga S., Grati M., Cohen-Salmon M., El-Amraoui A., Mustapha M., Salem N., El-Zir E., Loiselet J., Petit C. A mutation in OTOF, encoding Otoferlin, a FER-1-like protein, causes DFNB9, a nonsyndromic form of deafness. Nat. Gen. 1999, 21:363-369.
186. Yu X., Lewis E.R., Feld D. Seismic and auditory tuning curves from bullfrog saccular and amphibian papillar axons. J. Comp. Physiol. A 1991, 169:241-248.
187. Zenisek D., Davila V., Wan L., Almers W. Imaging calcium entry sites and ribbon structures in two presynaptic cells. J. Neurosci. 2003, 23:2538-2548.
188. Zhai R.G., Bellen H.J. The architecture of the active zone in the presynaptic nerve terminal. Physiology 2004, 19:262-270.
189. Rizzoli S.O., Betz W.J. The structural organization of the readily releasable pool of synaptic vesicles. Science 2004, 303:2037-2039.