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Hair cell ribbon synapses

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Abstract

Hearing and balance rely on the faithful synaptic coding of mechanical input by the auditory and vestibular hair cells of the inner ear. Mechanical deflection of their stereocilia causes the opening of mechanosensitive channels, resulting in hair cell depolarization, which controls the release of glutamate at ribbon-type synapses. Hair cells have a compact shape with strong polarity. Mechanoelectrical transduction and active membrane turnover associated with stereociliar renewal dominate the apical compartment. Transmitter release occurs at several active zones along the basolateral membrane. The astonishing capability of the hair cell ribbon synapse for temporally precise and reliable sensory coding has been the subject of intense investigation over the past few years. This research has been facilitated by the excellent experimental accessibility of the hair cell. For the same reason, the hair cell serves as an important model for studying presynaptic Ca2+ signaling and stimulus-secretion coupling. In addition to common principles, hair cell synapses differ in their anatomical and functional properties among species, among the auditory and vestibular organs, and among hair cell positions within the organ. Here, we briefly review synaptic morphology and connectivity and then focus on stimulus-secretion coupling at hair cell synapses.

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References

  • Art JJ, Fettiplace R (1987) Variation of membrane properties in hair cells isolated from the turtle cochlea. J Physiol (Lond) 385:207–242

    CAS  Google Scholar 

  • Art JJ, Crawford AC, Fettiplace R (1986) Electrical resonance and membrane currents in turtle cochlear hair cells. Hear Res 22:31–36

    Article  PubMed  CAS  Google Scholar 

  • Augustine GJ (2001) How does calcium trigger neurotransmitter release? Curr Opin Neurobiol 11:320–326

    Article  PubMed  CAS  Google Scholar 

  • Augustine GJ, Adler EM, Charlton MP (1991) The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann N Y Acad Sci 635:365–381

    Article  PubMed  CAS  Google Scholar 

  • Augustine GJ, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40:331–346

    Article  PubMed  CAS  Google Scholar 

  • Berglund AM, Ryugo DK (1987) Hair cell innervation by spiral ganglion neurons in the mouse. J Comp Neurol 255:560–570

    Article  PubMed  CAS  Google Scholar 

  • Beutner D, Voets T, Neher E, Moser T (2001) Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29:681–690

    Article  PubMed  CAS  Google Scholar 

  • Brandt A, Striessnig J, Moser T (2003) CaV1.3 channels are essential for development and presynaptic activity of cochlear inner hair cells. J Neurosci 23:10832–10840

    PubMed  CAS  Google Scholar 

  • Brandt A, Khimich D, Moser T (2005) Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25:11577–11585

    Article  PubMed  CAS  Google Scholar 

  • Brichta AM, Peterson EH (1994) Functional architecture of vestibular primary afferent from the posterior semicircular canal of the turtle, Pseudemys (Trachemys) scripta. J Comp Neurol 344:481–507

    Article  PubMed  CAS  Google Scholar 

  • Brichta AM, Goldberg JM (2000) Responses to efferent activation and excitatory response-intensity relations of turtle posterior-crista afferents. J Neurophysiol 83:1224–1242

    PubMed  CAS  Google Scholar 

  • Chang JS, Popper AN, Saidel WM (1992) Heterogeneity of sensory hair cells in a fish ear. J Comp Neurol 324:621–640

    Article  PubMed  CAS  Google Scholar 

  • Delgutte B (1980) Representation of speech-like sounds in the discharge patterns of auditory-nerve fibers. J Acoust Soc Am 68:843–857

    Article  PubMed  CAS  Google Scholar 

  • Desai SS, Ali H, Lysakowski A (2005a) Comparative morphology of rodent vestibular periphery. II. Cristae ampullares. J Neurophysiol 93:267–280

    Article  PubMed  Google Scholar 

  • Desai SS, Zeh C, Lysakowski A (2005b) Comparative morphology of rodent vestibular periphery. I. Saccular and utricular maculae. J Neurophysiol 93:251–266

    Article  PubMed  Google Scholar 

  • Dieck S tom, Brandstätter JH (2006) Retinal ribbon synapses. Cell Tissue Res (this issue, DOI 10.1007/s00441-006-0234-0)

  • Dou H, Vazquez AE, Namkung Y, Chu H, Cardell EL, Nie L, Parson S, Shin HS, Yamoah EN (2004) Null mutation of alpha1D Ca2+ channel gene results in deafness but no vestibular defect in mice. J Assoc Res Otolaryngol 5:215–226

    PubMed  Google Scholar 

  • Eatock RA, Hurley KM, Vollrath MA (2002) Mechanoelectrical and voltage-gated ion channels in mammalian vestibular hair cells. Audiol Neurootol 7:31–35

    Article  PubMed  CAS  Google Scholar 

  • Edmonds B, Reyes R, Schwaller B, Roberts WM (2000) Calretinin modifies presynaptic calcium signaling in frog saccular hair cells. Nat Neurosci 3:786–790

    Article  PubMed  CAS  Google Scholar 

  • Edmonds BW, Gregory FD, Schweizer FE (2004) Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells. J Physiol (Lond) 560:439–450

    Article  CAS  Google Scholar 

  • Engstrom H, Bergstrom B, Ades HW (1972) Macula utriculi and macula sacculi in the squirrel monkey. Acta Otolaryngol Suppl 301:75–126

    Article  PubMed  CAS  Google Scholar 

  • Eybalin M, Renard N, Aure F, Safieddine S (2002) Cysteine-string protein in inner hair cells of the organ of Corti: synaptic expression and upregulation at the onset of hearing. Eur J Neurosci 15:1409–1420

    Article  PubMed  Google Scholar 

  • Fernandez C, Baird RA, Goldberg JM (1988) The vestibular nerve of the chinchilla. I. Peripheral innervation patterns in the horizontal and superior semicircular canals. J Neurophysiol 60:167–181

    PubMed  CAS  Google Scholar 

  • Fernandez C, Goldberg JM, Baird RA (1990) The vestibular nerve of the chinchilla. III. Peripheral innervation patterns in the utricular macula. J Neurophysiol 63:767–780

    PubMed  CAS  Google Scholar 

  • Fernandez C, Lysakowski A, Goldberg JM (1995) Hair-cell counts and afferent innervation patterns in the cristae ampullares of the squirrel monkey with a comparison to the chinchilla. J Neurophysiol 73:1253–1269

    PubMed  CAS  Google Scholar 

  • Fettiplace R (1992) The role of calcium in hair cell transduction. Soc Gen Physiol Ser 47:343–356

    PubMed  CAS  Google Scholar 

  • Fischer FP (1992) Quantitative analysis of the innervation of the chicken basilar papilla. Hear Res 61:167–178

    Article  PubMed  CAS  Google Scholar 

  • Francis HW, Rivas A, Lehar M, Ryugo DK (2004) Two types of afferent terminals innervate cochlear inner hair cells in C57BL/6J mice. Brain Res 1016:182–194

    Article  PubMed  CAS  Google Scholar 

  • Fuchs PA, Nagai T, Evans MG (1988) Electrical tuning in hair cells isolated from the chick cochlea. J Neurosci 8:2460–2467

    PubMed  CAS  Google Scholar 

  • Fuchs PA, Evans MG, Murrow BW (1990) Calcium currents in hair cells isolated from the cochlea of the chick. J Physiol (Lond) 429:553–568

    Google Scholar 

  • Furness DN, Lawton DM (2003) Comparative distribution of glutamate transporters and receptors in relation to afferent innervation density in the mammalian cochlea. J Neurosci 23:11296–11304

    PubMed  CAS  Google Scholar 

  • Furness DN, Lehre KP (1997) Immunocytochemical localization of a high-affinity glutamate-aspartate transporter, GLAST, in the rat and guinea-pig cochlea. Eur J Neurosci 9:1961–1969

    Article  PubMed  CAS  Google Scholar 

  • Furukawa T (1986) Sound reception and synaptic transmission in goldfish hair cells. Jpn J Physiol 36:1059–1077

    Article  PubMed  CAS  Google Scholar 

  • Furukawa T, Matsuura S (1978) Adaptive rundown of excitatory post-synaptic potentials at synapses between hair cells and eight nerve fibres in the goldfish. J Physiol (Lond) 276:193–209

    CAS  Google Scholar 

  • Glowatzki E, Fuchs PA (2002) Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5:147–154

    Article  PubMed  CAS  Google Scholar 

  • Goldberg JM, Lysakowski A, Fernandez C (1990) Morphophysiological and ultrastructural studies in the mammalian cristae ampullares. Hear Res 49:89–102

    Article  PubMed  CAS  Google Scholar 

  • Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130:277–297

    Article  PubMed  CAS  Google Scholar 

  • Griesinger CB, Richards CD, Ashmore JF (2005) Fast vesicle replenishment allows indefatigable signalling at the first auditory synapse. Nature 435:212–215

    Article  PubMed  CAS  Google Scholar 

  • Hackney CM, Mahendrasingam S, Jones EM, Fettiplace R (2003) The distribution of calcium buffering proteins in the turtle cochlea. J Neurosci 23:4577–4589

    PubMed  CAS  Google Scholar 

  • Hackney CM, Mahendrasingam S, Penn A, Fettiplace R (2005) The concentrations of calcium buffering proteins in mammalian cochlear hair cells. J Neurosci 25:7867–7875

    Article  PubMed  CAS  Google Scholar 

  • Hafidi A, Beurg M, Dulon D (2005) Localization and developmental expression of BK channels in mammalian cochlear hair cells. Neuroscience 130:475–484

    Article  PubMed  CAS  Google Scholar 

  • Hakuba N, Koga K, Shudou M, Watanabe F, Mitani A, Gyo K (2000) Hearing loss and glutamate efflux in the perilymph following transient hindbrain ischemia in gerbils. J Comp Neurol 418:217–226

    Article  PubMed  CAS  Google Scholar 

  • Heller S, Bell AM, Denis CS, Choe Y, Hudspeth AJ (2002) Parvalbumin 3 is an abundant Ca2+ buffer in hair cells. J Assoc Res Otolaryngol 3:488–498

    Article  PubMed  Google Scholar 

  • Holt JC, Xue JT, Brichta AM, Goldberg JM (2006) Transmission between type II hair cells and bouton afferents in the turtle posterior crista. J Neurophysiol 95:428–452

    Article  PubMed  Google Scholar 

  • Issa NP, Hudspeth AJ (1994) Clustering of Ca2+ channels and Ca2+-activated K+ channels at fluorescently labeled presynaptic active zones of hair cells. Proc Natl Acad Sci USA 91:7578–7582

    Article  PubMed  CAS  Google Scholar 

  • Johnson SL, Marcotti W, Kros CJ (2005) Increase in efficiency and reduction in Ca2+ dependence of exocytosis during development of mouse inner hair cells. J Physiol (Lond) 563:177–191

    Article  CAS  Google Scholar 

  • Keen EC, Hudspeth AJ (2006) Transfer characteristics of the hair cell’s afferent synapse. Proc Natl Acad Sci USA 103:5537–5542

    Article  PubMed  CAS  Google Scholar 

  • Kennedy HJ, Crawford AC, Fettiplace R (2005) Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 433:880–883

    Article  PubMed  CAS  Google Scholar 

  • Kharkovets T, Dedek K, Maier H, Schweizer M, Khimich D, Nouvian R, Vardanyan V, Leuwer R, Moser T, Jentsch TJ (2006) Mice with altered KCNQ4 K+ channels implicate sensory outer hair cells in human progressive deafness. EMBO J 25:642–652

    Article  PubMed  CAS  Google Scholar 

  • Khimich D, Nouvian R, Pujol R, Tom Dieck S, Egner A, Gundelfinger ED, Moser T (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434:889–894

    Article  PubMed  CAS  Google Scholar 

  • Kiang NY-S, Watanabe T, Thomas EC, Clark LF (1965) Discharge pattern of single fibers in the cat’s auditory nerve. MIT Press, Cambridge

    Google Scholar 

  • Kimura RS (1984) Sensory and accessory epithelia of the cochlea. In: Friedemann I, Ballantyne J (eds) Ultrastructural atlas of the inner ear. Butterworths, London, pp 101–132

    Google Scholar 

  • Koschak A, Reimer D, Huber I, Grabner M, Glossmann H, Engel J, Striessnig J (2001) Alpha 1D (Cav1.3) subunits can form L-type Ca2+ channels activating at negative voltages. J Biol Chem 276:22100–22106

    Article  PubMed  CAS  Google Scholar 

  • Kros CJ (1996) Physiology of mammalian cochlea hair cells. In: Dallos P, et al (eds) The cochlea. Springer, Berlin Heidelberg New York, pp 318–385

    Google Scholar 

  • Kubisch C, Schroeder BC, Friedrich T, Lutjohann B, El-Amraoui A, Marlin, S, Petit C, Jentsch TJ (1999) KCNQ4, a novel potassium channel expressed in sensory outer hair cells, is mutated in dominant deafness. Cell 96:437–446

    Article  PubMed  CAS  Google Scholar 

  • Lenzi D, Roberts WM (1994) Calcium signalling in hair cells: multiple roles in a compact cell. Curr Opin Neurobiol 4:496–502

    Article  PubMed  CAS  Google Scholar 

  • Lenzi D, Runyeon JW, Crum J, Ellisman MH, Roberts WM (1999) Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J Neurosci 19:119–132

    PubMed  CAS  Google Scholar 

  • Lewis RS, Hudspeth AJ (1983) Voltage- and ion-dependent conductances in solitary vertebrate hair cells. Nature 304:538–541

    Article  PubMed  CAS  Google Scholar 

  • Liberman MC (1980) Morphological differences among radial afferent fibers in the cat cochlea: an electron-microscopic study of serial sections. Hear Res 3:45–63

    Article  PubMed  CAS  Google Scholar 

  • Liberman MC (1982) Single-neuron labeling in cat auditory nerve. Science 216:1239–1241

    Article  PubMed  CAS  Google Scholar 

  • Liberman MC, Kiang NY (1978) Acoustic trauma in cats. Cochlear pathology and auditory-nerve activity. Acta Otolaryngol Suppl 358:1–63

    PubMed  CAS  Google Scholar 

  • Liberman MC, Dodds LW, Pierce S (1990) Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy [erratum in J Comp Neurol (1991) 304:341]. J Comp Neurol 301:443–460

    Article  PubMed  CAS  Google Scholar 

  • Lysakowski A (1996) Synaptic organization of the crista ampullaris in vertebrates. Ann N Y Acad Sci 781:164–182

    Article  PubMed  CAS  Google Scholar 

  • Lysakowski A, Goldberg JM (1997) A regional ultrastructural analysis of the cellular and synaptic architecture in the chinchilla cristae ampullares. J Comp Neurol 389:419–443

    Article  PubMed  CAS  Google Scholar 

  • Marcotti W, Johnson SL, Kros CJ (2004) Effects of intracellular stores and extracellular Ca(2+) on Ca(2+)-activated K(+) currents in mature mouse inner hair cells. J Physiol (Lond) 557:613–633

    Article  CAS  Google Scholar 

  • Martinez-Dunst C, Michaels RL, Fuchs PA (1997) Release sites and calcium channels in hair cells of the chick’s cochlea. J Neurosci 17:9133–9144

    PubMed  CAS  Google Scholar 

  • Martini M, Rossi ML, Rubbini G, Rispoli G (2000) Calcium currents in hair cells isolated from semicircular canals of the frog. Biophys J 78:1240–1254

    Article  PubMed  CAS  Google Scholar 

  • Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP (1996) 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 16:4457–4467

    PubMed  CAS  Google Scholar 

  • Merchan-Perez A, Liberman MC (1996) Ultrastructural differences among afferent synapses on cochlear hair cells: correlations with spontaneous discharge rate. J Comp Neurol 371:208–221

    Article  PubMed  CAS  Google Scholar 

  • Michna M, Knirsch M, Hoda JC, Muenkner S, Langer P, Platzer J, Striessnig J, Engel J (2003) Cav1.3 (alpha1D) Ca2+ currents in neonatal outer hair cells of mice. J Physiol (Lond) 553:747–758

    Article  CAS  Google Scholar 

  • Mintz IM, Sabatini BL, Regehr WG (1995) Calcium control of transmitter release at a cerebellar synapse. Neuron 15:675–688

    Article  PubMed  CAS  Google Scholar 

  • Moser T, Beutner D (2000) Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci USA 97:883–888

    Article  PubMed  CAS  Google Scholar 

  • Nemzou RM, Bulankina AV, Khimich D, Giese A, Moser T (2006) Synaptic organization in CaV1.3 Ca2+ channel deficient cochlear hair cells. Neuroscience (in press) DOI 10.1016/j.neuroscience.2006.05.057

  • Nouvian R, Ruel J, Wang J, Guitton MJ, Pujol R, Puel JL (2003) Degeneration of sensory outer hair cells following pharmacological blockade of cochlear KCNQ channels in the adult guinea pig. Eur J Neurosci 17:2553–2562

    Article  PubMed  Google Scholar 

  • Nouvian R, Beutner D, Parsons TD, Moser T (2006) Structure and function of the hair cell ribbon synapse. J Membr Biol 209:153–165

    Article  PubMed  CAS  Google Scholar 

  • Oliver D, Taberner AM, Thurm H, Sausbier M, Arntz C, Ruth P, Fakler B, Liberman MC (2006) The role of BKCa channels in electrical signal encoding in the mammalian auditory periphery. J Neurosci 26:6181–6189

    Article  PubMed  CAS  Google Scholar 

  • Parsons TD, Lenzi D, Almers W, Roberts WM (1994) Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 13:875–883

    Article  PubMed  CAS  Google Scholar 

  • Platzer J, Engel J, Schrott-Fischer A, Stephan K, Bova S, Chen H, Zheng H, Striessnig J (2000) Congenital deafness and sinoatrial node dysfunction in mice lacking class D L-type Ca2+ channels. Cell 102:89–97

    Article  PubMed  CAS  Google Scholar 

  • Pyott SJ, Glowatzki E, Trimmer JS, Aldrich RW (2004) Extrasynaptic localization of inactivating calcium-activated potassium channels in mouse inner hair cells. J Neurosci 24:9469–9474

    Article  PubMed  CAS  Google Scholar 

  • Ricci AJ, Wu YC, Fettiplace R (1998) The endogenous calcium buffer and the time course of transducer adaptation in auditory hair cells. J Neurosci 18:8261–8277

    PubMed  CAS  Google Scholar 

  • Roberts WM (1993) Spatial calcium buffering in saccular hair cells. Nature 363:74–76

    Article  PubMed  CAS  Google Scholar 

  • Roberts WM (1994) Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci 14:3246–3262

    PubMed  CAS  Google Scholar 

  • Roberts WM, Jacobs RA, Hudspeth AJ (1990) Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci 10:3664–3684

    PubMed  CAS  Google Scholar 

  • Robertson D, Paki B (2002) Role of L-type Ca2+ channels in transmitter release from mammalian inner hair cells. II. Single-neuron activity. J Neurophysiol 87:2734–2740

    PubMed  CAS  Google Scholar 

  • Rodriguez-Contreras A, Yamoah EN (2001) Direct measurement of single-channel Ca(2+) currents in bullfrog hair cells reveals two distinct channel subtypes. J Physiol (Lond) 534:669–689

    Article  CAS  Google Scholar 

  • Rodriguez-Contreras A, Nonner W, Yamoah EN (2002) Ca2+ transport properties and determinants of anomalous mole fraction effects of single voltage-gated Ca2+ channels in hair cells from bullfrog saccule. J Physiol (Lond) 538:729–745

    Article  CAS  Google Scholar 

  • Rose JE, Brugge JF, Anderson DJ, Hind JE (1967) Phase-locked response to low frequency tones in single auditory nerve fibers of the squirrel monkey. J Neurophysiol 30:769–793

    PubMed  CAS  Google Scholar 

  • Rutherford MA, Roberts WM (2006) Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proc Natl Acad Sci USA 103:2898–2903

    Article  PubMed  CAS  Google Scholar 

  • Ruttiger L, Sausbier M, Zimmermann U, Winter H, Braig C, Engel J, Knirsch M, Arntz C, Langer P, Hirt B, Muller M, Kopschall I, Pfister M, Munkner S, Rohbock K, Pfaff I, Rusch A, Ruth P, Knipper M (2004) Deletion of the Ca2+-activated potassium (BK) alpha-subunit but not the BKbeta1-subunit leads to progressive hearing loss. Proc Natl Acad Sci USA 101:12922–12927

    Article  PubMed  Google Scholar 

  • Safieddine S, Wenthold RJ (1999) SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle- and synaptic membrane-associated proteins. Eur J Neurosci 11:803–812

    Article  PubMed  CAS  Google Scholar 

  • Saito K (1980) Fine structure of the sensory epithelium of the guinea pig organ of Corti: afferent and efferent synapses of hair cells. J Ultrastruc Res 71:222–232

    Article  CAS  Google Scholar 

  • Schnee ME, Lawton DM, Furness DN, Benke TA, Ricci AJ (2005) Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47:243–254

    Article  PubMed  CAS  Google Scholar 

  • Schneggenburger R, Forsythe ID (2006) The calyx of Held. Cell Tissue Res (this issue, 10.1007/s00441-006-0272-7)

  • Schwaller B, Meyer M, Schiffmann S (2002) “New” functions for “old” proteins: the role of the calcium-binding proteins calbindin D-28k, calretinin and parvalbumin, in cerebellar physiology. Studies with knockout mice. Cerebellum 1:241–258

    Article  PubMed  CAS  Google Scholar 

  • Sewell WF (1984) The relation between the endocochlear potential and spontaneous activity in auditory nerve fibres of the cat. J Physiol (Lond) 347:685–696

    CAS  Google Scholar 

  • Sidi S, Busch-Nentwich E, Friedrich R, Schoenberger U, Nicolson T (2004) Gemini encodes a zebrafish L-type calcium channel that localizes at sensory hair cell ribbon synapses. J Neurosci 24:4213–4223

    Article  PubMed  CAS  Google Scholar 

  • Slepecky NB, Galsky MD, Swartzentruber-Martin H, Savage J (2000) Study of afferent nerve terminals and fibers in gerbil cochlea: distribution by size. Hear Res 144:124–134

    Article  PubMed  CAS  Google Scholar 

  • Sneary MG (1988) Auditory receptor of the red-eared turtle. II. Afferent and efferent synapses and innervation patterns. J Comp Neurol 276:588–606

    Article  PubMed  CAS  Google Scholar 

  • Spassova M, Eisen MD, Saunders JC, Parsons TD (2001) Chick cochlear hair cell exocytosis mediated by dihydropyridine-sensitive calcium channels. J Physiol (Lond) 535:689–696

    Article  CAS  Google Scholar 

  • Spassova MA, Avissar M, Furman AC, Crumling MA, Saunders JC, Parsons TD (2004) Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse. J Assoc Res Otolaryngol 5:376–390

    Article  PubMed  Google Scholar 

  • Spicer SS, Salvi RJ, Schulte BA (1999) Ablation of inner hair cells by carboplatin alters cells in the medial K(+) flow route and disrupts tectorial membrane. Hear Res 136:139–150

    Article  PubMed  CAS  Google Scholar 

  • Thurm H, Fakler B, Oliver D (2005) Ca2+-independent activation of BKCa channels at negative potentials in mammalian inner hair cells. J Physiol (Lond) 569:137–151

    Article  CAS  Google Scholar 

  • Tsuji J, Liberman MC (1997) Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J Comp Neurol 381:188–202

    Article  PubMed  CAS  Google Scholar 

  • Tucker T, Fettiplace R (1995) Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells. Neuron 15:1323–1335

    Article  PubMed  CAS  Google Scholar 

  • Tucker TR, Fettiplace R (1996) Monitoring calcium in turtle hair cells with a calcium-activated potassium channel. J Physiol (Lond) 494:613–626

    CAS  Google Scholar 

  • Wegner N (1982) A qualitative and quantitative study of a sensory epithelium in the inner ear of a fish (Colisa labiosa; Anabantidae). Acta Zoologica 63:133–146

    Article  Google Scholar 

  • Wong WH, Hurley KM, Eatock RA (2004) Differences between the negatively activating potassium conductances of mammalian cochlear and vestibular hair cells. J Assoc Res Otolaryngol 5:270–284

    Article  PubMed  Google Scholar 

  • Wu YC, Art JJ, Goodman MB, Fettiplace R (1995) A kinetic description of the calcium-activated potassium channel and its application to electrical tuning of hair cells. Prog Biophys Mol Biol 63:131–158

    Article  PubMed  CAS  Google Scholar 

  • Xu W, Lipscombe D (2001) Neuronal Ca(V)1.3alpha(1) L-type channels activate at relatively hyperpolarized membrane potentials and are incompletely inhibited by dihydropyridines. J Neurosci 21:5944–5951

    PubMed  CAS  Google Scholar 

  • Yasunaga S, Grati M, Cohen-Salmon M, El-Amraoui A, Mustapha M, Salem N, El-Zir E, Loiselet J, Petit C (1999) A mutation in OTOF, encoding otoferlin, a FER-1-like protein, causes DFNB9, a nonsyndromic form of deafness. Nat Genet 21:363–369

    Article  PubMed  CAS  Google Scholar 

  • Zenisek D, Davila V, Wan L, Almers W (2003) Imaging calcium entry sites and ribbon structures in two presynaptic cells. J Neurosci 23:2538–2548

    PubMed  CAS  Google Scholar 

  • Zhang SY, Robertson D, Yates G, Everett A (1999) Role of L-type Ca(2+) channels in transmitter release from mammalian inner hair cells. I. Gross sound-evoked potentials. J Neurophysiol 82:3307–3315

    PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Regis Nouvian, Alexander Meyer and Beat Schwaller for comments on the manuscript, William Roberts for providing figures of his microdomain modeling, Ruth Anne Eatock for discussion on Ca2+ channels in mammalian vestibular hair cells, and Gerhard Hoch and Steven D. Price for excellent technical assistance.

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  1. Department of Otolaryngology and Center for Molecular Physiology of the Brain, University of Göttingen, Robert-Koch-Strasse 40, 37075, Göttingen, Germany

    Tobias Moser & Andreas Brandt

  2. Department of Anatomy & Cell Biology, University of Illinois at Chicago, Chicago, IL 60612, USA

    Anna Lysakowski

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  1. Tobias Moser
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  2. Andreas Brandt
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  3. Anna Lysakowski
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Correspondence to Tobias Moser.

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Research at the Moser laboratory was supported by grants from the DFG (SFB406 and CMPB), the European Commission (through the integrated project EuroHear), the Human Frontiers Science Program (HFSP), and the Federal Goverment (through the Bernstein Center for Computational Neuroscience, Göttingen). Research at the Lysakowski laboratory was supported by grants from NIH (R01 DC02521, R01 DC02290, and R01 DC002358) and the American Hearing Research Foundation.

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Moser, T., Brandt, A. & Lysakowski, A. Hair cell ribbon synapses. Cell Tissue Res 326, 347–359 (2006). https://doi.org/10.1007/s00441-006-0276-3

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