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  • Review Article
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The sensory and motor roles of auditory hair cells

Nature Reviews Neuroscience volume 7, pages 19–29 (2006)Cite this article

Key Points

  • Sound vibrations conducted to the cochlea are detected by inner and outer hair cells. Both types of hair cell transduce sound stimuli through minute displacements of their hair bundle, an array of modified microvilli known as stereocilia that project from their apical surface.

  • Outer hair cells, unlike inner hair cells, have a further role in generating force, known as the cochlear amplifier, which mechanically boosts the sound-induced vibrations and augments frequency tuning. Two mechanisms of force generation have been advanced: contractions of the cell soma and active motion of the hair bundle.

  • Many proteins found in the mechanosensory hair bundle have been isolated by studies of genetic mutations that cause deafness. Crucial proteins for hair bundle development and function include many myosin isoforms.

  • Myosin XVa is localized to the tips of the stereocilia and might regulate the rate of actin incorporation, and thereby specify stereociliary length. Myosin VIIa might control the interciliary linkages, whereas myosin 1c is proposed to modulate the force on the mechanotransducer channel imposed by stretch of the tip links.

  • Deflections of the hair bundle are detected by mechanoelectrical transduction (MET) channels, which are located at the tips of stereocilia and activated by tension in the tip links. The most likely candidate for the MET channels is a transient receptor potential (TRP) channel, possibly TRPA1, which has large unitary conductance and is highly permeable to Ca2+.

  • Elevation of intracellular Ca2+ by influx of the ion through MET channels controls adaptation by various routes, including fast channel re-closure and slower control of the force imposed on the channel through myosin 1c.

  • Fast adaptation of the MET channels occurs on a submillisecond timescale. Hair cells tuned to higher frequencies have MET channels with larger single-channel conductance, permitting a larger Ca2+ influx and faster adaptation matched to the frequency detected by the hair cell.

  • One mode of force generation by outer hair cells occurs by voltage-dependent contractions of the cell soma attributable to the chloride-binding protein prestin. However, prestin might not operate on a cycle-by-cycle basis at high frequencies because the receptor potential is attenuated by the membrane time constant.

  • Recent results indicate that changes in MET channel gating attributable to fast adaptation cause force generation by the hair bundle that could supplement prestin-driven somatic contractions. Prestin's role might then be to act as another form of adaptation, continuously resetting the operating range of the MET channels to maintain them in their most sensitive position.

Abstract

Cochlear hair cells respond with phenomenal speed and sensitivity to sound vibrations that cause submicron deflections of their hair bundle. Outer hair cells are not only detectors, but also generate force to augment auditory sensitivity and frequency selectivity. Two mechanisms of force production have been proposed: contractions of the cell body or active motion of the hair bundle. Here, we describe recently identified proteins involved in the sensory and motor functions of auditory hair cells and present evidence for each force generator. Both motor mechanisms are probably needed to provide the high sensitivity and frequency discrimination of the mammalian cochlea.

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Figure 1: The sound conduction pathway.
Figure 2: Cellular structure of the sound-detecting organ of Corti.
Figure 3: Structure and protein composition of the stereociliary bundle.
Figure 4: Mechanoelectrical tranduction currents in outer hair cells.
Figure 5: The putative motors of outer hair cells.
Figure 6: Mechanical properties of an outer hair cell bundle.

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References

  1. Von Békésy, G. Experiments in Hearing (McGraw-Hill, New York, 1960).

    Google Scholar 

  2. Geisler, C. D. From Sound to Synapse (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  3. Hudspeth, A. J. How the ear's works work. Nature 341, 397–404 (1989).

    Article  CAS  PubMed  Google Scholar 

  4. Dallos, P. The active cochlea. J. Neurosci. 12, 4575–4585 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Manley, G. A. Cochlear mechanisms from a phylogenetic viewpoint. Proc. Natl Acad. Sci. USA 97, 11736–11743 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Friedman, T. B. & Griffith, A. J. Human nonsyndromic sensorineural deafness. Annu. Rev. Genomics Hum. Genet. 4, 341–402 (2003).

    Article  CAS  PubMed  Google Scholar 

  7. Shotwell, S. L., Jacobs, R. & Hudspeth, A. J. Directional sensitivity of individual vertebrate hair cells to controlled deflection of their hair bundles. Ann. NY Acad. Sci. 374, 1–10 (1981).

    Article  CAS  PubMed  Google Scholar 

  8. Furness, D. N., Katori, Y., Mahendrasingam, S. & Hackney, C. M. Differential distribution of β- and γ-actin in guinea-pig cochlear sensory and supporting cells. Hear. Res. 207, 22–34 (2005).

    Article  CAS  PubMed  Google Scholar 

  9. Tilney, L. G. & Tilney, M. S. Functional organization of the cytoskeleton. Hear. Res. 22, 55–77 (1986).

    Article  CAS  PubMed  Google Scholar 

  10. Bartles, J. R. Parallel actin bundles and their multiple actin-binding proteins. Curr. Opin. Cell Biol. 12, 72–78 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Pataky, F., Pironkova, R. & Hudspeth, A. J. Radixin is a constituent of stereocilia in hair cells. Proc. Natl Acad. Sci. USA 101, 2601–2606 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Slepecky, N. & Chamberlain, S. C. Immunoelectron microscopic and immunofluorescent localization of cytoskeletal and muscle-like contractile proteins in inner ear sensory hair cells. Hear. Res. 20, 245–260 (1985).

    Article  CAS  PubMed  Google Scholar 

  13. Hackney, C. M., Karkanevatos, A. & Furness, D. N. Distribution of tropomyosin in guinea pig cochlear hair cells. J. Physiol. (Lond.) 527, 92P (2000).

    Google Scholar 

  14. Schneider, M. E., Belyantseva, I. A., Azevedo, R. B. & Kachar, B. Rapid renewal of auditory hair bundles. Nature 418, 837–838 (2002).

    Article  CAS  PubMed  Google Scholar 

  15. Rzadzinska, A. K., Schneider, M. E., Davies, C., Riordan, G. P. & Kachar, B. An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J. Cell Biol. 164, 887–897 (2004). Shows treadmilling of actin along the stereocilia at a rate proportional to their length and proposes that myosin XVa that is localized at stereociliary tips regulates treadmilling rate and stereociliary length.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Belyantseva, I. A. et al. Myosin-XVa is required for tip localization of whirlin and differential elongation of hair-cell stereocilia. Nature Cell Biol. 7, 148–156 (2005).

    Article  CAS  PubMed  Google Scholar 

  17. Mburu, P. et al. Defects in whirlin, a PDZ domain molecule involved in stereocilia elongation, cause deafness in the whirler mouse and families with DFNB31. Nature Genet. 34, 421–428 (2003).

    Article  CAS  PubMed  Google Scholar 

  18. Pickles, J. O., Comis, S. D. & Osborne, M. P. Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hear. Res. 15, 103–112 (1984).

    Article  CAS  PubMed  Google Scholar 

  19. Furness, D. N. & Hackney, C. M. Cross-links between stereocilia in the guinea pig cochlea. Hear. Res. 18, 177–188 (1985).

    Article  CAS  PubMed  Google Scholar 

  20. Goodyear, R. J., Marcotti, W., Kros, C. J. & Richardson, G. P. Development and properties of stereociliary link types in hair cells of the mouse cochlea. J. Comp. Neurol. 485, 75–85 (2005).

    Article  PubMed  Google Scholar 

  21. Flock, A., Flock, B. & Murray, E. Studies on the sensory hairs of receptor cells in the inner ear. Acta Otolaryngol. 83, 85–91 (1977).

    Article  CAS  PubMed  Google Scholar 

  22. Boeda, B. et al. Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair bundle. EMBO J. 21, 6689–6699 (2002). Evidence that interactions between three Usher I gene products are important for hair bundle morphogenesis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kros, C. J. et al. Reduced climbing and increased slipping adaptation in cochlear hair cells of mice with Myo7a mutations. Nature Neurosci. 5, 41–47 (2002).

    Article  CAS  PubMed  Google Scholar 

  24. Assad, J. A., Shepherd, G. M. & Corey, D. P. Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7, 985–994 (1991).

    Article  CAS  PubMed  Google Scholar 

  25. Crawford, A. C., Evans, M. G. & Fettiplace, R. The actions of calcium on the mechano-electrical transducer current of turtle hair cells. J. Physiol. (Lond.) 434, 369–398 (1991).

    Article  CAS  Google Scholar 

  26. Denk, W., Holt, J. R., Shepherd, G. M. & Corey, D. P. Calcium imaging of single stereocilia in hair cells: localization of transduction channels at both ends of tip links. Neuron 15, 1311–1321 (1995).

    Article  CAS  PubMed  Google Scholar 

  27. Lumpkin, E. A. & Hudspeth, A. J. Detection of Ca2+ entry through mechanosensitive channels localizes the site of mechanoelectrical transduction in hair cells. Proc. Natl Acad. Sci. USA 92, 10297–10301 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Siemens, J. et al. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428, 950–955 (2004).

    Article  CAS  PubMed  Google Scholar 

  29. Söllner, C. et al. Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428, 955–959 (2004).

    Article  PubMed  CAS  Google Scholar 

  30. Michel, V. et al. Cadherin 23 is a component of the transient lateral links in the developing hair bundles of cochlear sensory cells. Dev. Biol. 280, 281–294 (2005).

    Article  CAS  PubMed  Google Scholar 

  31. Lagziel, A. et al. Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development. Dev. Biol. 280, 295–306 (2005).

    Article  CAS  PubMed  Google Scholar 

  32. Robles, L. & Ruggero, M. A. Mechanics of the mammalian cochlea. Physiol. Rev. 81, 1305–1352 (2001). Comprehensive review of the measurements and mechanisms of the mechanical frequency tuning of the basilar membrane.

    Article  CAS  PubMed  Google Scholar 

  33. Hu, X., Evans, B. N. & Dallos, P. Direct visualization of organ of Corti kinematics in a hemicochlea. J. Neurophysiol. 82, 2798–2807 (1999).

    Article  CAS  PubMed  Google Scholar 

  34. Ohmori, H. Mechano-electrical transduction currents in isolated vestibular hair cells of the chick. J. Physiol. (Lond.) 359, 189–217 (1985).

    Article  CAS  Google Scholar 

  35. Ricci, A. J. & Fettiplace, R. Calcium permeation of the turtle hair cell mechanotransducer channel and its relation to the composition of endolymph. J. Physiol. (Lond.) 506, 159–173 (1998).

    Article  CAS  Google Scholar 

  36. Farris, H. E., LeBlanc, C. L., Goswami, J. & Ricci, A. J. Probing the pore of the auditory hair cell mechanotransducer channel in turtle. J. Physiol. (Lond.) 558, 769–792 (2004).

    Article  CAS  Google Scholar 

  37. Ricci, A. J., Crawford, A. C. & Fettiplace, R. Tonotopic variation in the conductance of the hair cell mechanotransducer channel. Neuron 40, 983–990 (2003). Uses the destruction of tip links with BAPTA to record single MET channels, showing their variation in conductance along the cochlea.

    Article  CAS  PubMed  Google Scholar 

  38. Géléoc, G. S., Lennan, G. W., Richardson, G. P. & Kros, C. J. A quantitative comparison of mechanoelectrical transduction in vestibular and auditory hair cells of neonatal mice. Proc. R. Soc. Lond. B 264, 611–621 (1997).

    Article  Google Scholar 

  39. Corey, D. P. & Hudspeth, A. J. Kinetics of the receptor current in bullfrog saccular hair cells. J. Neurosci. 3, 962–976 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Crawford, A. C., Evans, M. G. & Fettiplace, R. Activation and adaptation of transducer currents in turtle hair cells. J. Physiol. (Lond.) 419, 405–434 (1989).

    Article  CAS  Google Scholar 

  41. Eatock, R. A. Adaptation in hair cells. Annu. Rev. Neurosci. 23, 285–314 (2000).

    Article  CAS  PubMed  Google Scholar 

  42. Ricci, A. J., Wu, Y. -C. & Fettiplace, R. The endogenous calcium buffer and the time course of transducer adaptation in auditory hair cells. J. Neurosci. 18, 8261–8277 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kros, C. J., Rüsch, A. & Richardson, G. P. Mechano-electrical transducer currents in hair cells of the cultured neonatal mouse cochlea. Proc. R. Soc. Lond. B 249, 185–193 (1992). Reports the first use of an isolated mammalian cochlear preparation to record large transducer currents.

    Article  CAS  Google Scholar 

  44. Kennedy, H. J., Evans, M. G., Crawford, A. C. & Fettiplace, R. Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells. Nature Neurosci. 6, 832–836 (2003).

    Article  CAS  PubMed  Google Scholar 

  45. He, D. Z. Z., Jia, S. & Dallos, P. Mechanoelectrical transduction of adult outer hair cells studied in a gerbil cochlea. Nature 429, 766–770 (2004).

    Article  CAS  PubMed  Google Scholar 

  46. Ricci, A. J., Kennedy, H. J., Crawford, A. C. & Fettiplace, R. The transduction channel filter in auditory hair cells. J. Neurosci. 25, 7831–7839 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Dumont, R. A. et al. Plasma membrane Ca2+-ATPase isoform 2a is the PMCA of hair bundles. J. Neurosci. 21, 5066–5078 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Martin, P., Bozovic, D., Choe, Y. & Hudspeth, A. J. Spontaneous oscillation by hair bundles of the bullfrog's sacculus. J. Neurosci. 23, 4533–4548 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Gillespie, P. G. & Cyr, J. L. Myosin-1c, the hair cell's adaptation motor. Annu. Rev. Physiol. 66, 521–545 (2004).

    Article  CAS  PubMed  Google Scholar 

  51. Holt, J. R. et al. A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108, 371–381 (2002). Mutation of myosin-1c to confer selectivity to block by ADP analogues unequivocally shows the role of the motor protein in hair cell adaptation.

    Article  CAS  PubMed  Google Scholar 

  52. Stauffer, E. A. et al. Fast adaptation in vestibular hair cells requires myosin-1c activity. Neuron 47, 541–553 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Pedersen, S. F., Owsianik, G. & Nilius, B. TRP channels: an overview. Cell Calcium 38, 233–252 (2005).

    Article  CAS  PubMed  Google Scholar 

  54. Corey, D. P. et al. TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432, 723–730 (2004). Identification of the most plausible candidate for the long sought-after MET channel protein.

    Article  CAS  PubMed  Google Scholar 

  55. Story, G. M. et al. ANKTM1, a TRP-like channel expressed in nociceptive neurons is activated at cold temperatures. Cell 112, 819–829 (2003).

    Article  CAS  PubMed  Google Scholar 

  56. Nagata, K., Duggan, A., Kumar, G. & Garcia-Anoveros, J. Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J. Neurosci. 25, 4052–4061 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Schaefer, M. Homo- and heteromeric assembly of TRP channel subunits. Pflugers Arch. 451, 35–42 (2005).

    Article  CAS  PubMed  Google Scholar 

  58. Di Palma, F. et al. Mutations in Mcoln3 associated with deafness and pigmentation defects in varitint-waddler (Va) mice. Proc. Natl Acad. Sci. USA 99, 14994–14999 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Hirono, M., Denis, C. S., Richardson, G. P. & Gillespie, P. G. Hair cells require phosphatidylinositol 4,5-bisphosphate for mechanical transduction and adaptation. Neuron 44, 309–320 (2004).

    Article  CAS  PubMed  Google Scholar 

  60. Kachar, B., Parakka, l. M., Kurc, M., Zhao, Y. & Gillespie, P. G. High-resolution structure of hair-cell tip links. Proc. Natl Acad. Sci. USA 97, 13336–13341 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Howard, J. & Hudspeth, A. J. Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron 1, 189–199 (1988). First demonstration of and elegant theory for the contribution of MET channel gating to hair bundle mechanics.

    Article  CAS  PubMed  Google Scholar 

  62. Russell, I. J., Kössl, M. & Richardson, G. P. Nonlinear mechanical responses of mouse cochlear hair bundles. Proc. R. Soc. Lond. B 250, 217–227 (1992).

    Article  CAS  Google Scholar 

  63. van Netten, S. M. & Kros, C. J. Gating energies and forces of the mammalian hair cell transducer channel and related hair bundle mechanics. Proc. R. Soc. Lond. B 267, 1915–1923 (2000).

    Article  CAS  Google Scholar 

  64. Ricci, A. J., Crawford, A. C. & Fettiplace, R. Mechanisms of active hair bundle motion in auditory hair cells. J. Neurosci. 22, 44–52 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Benser, M. E., Marquis, R. E. & Hudspeth, A. J. Rapid, active hair bundle movements in hair cells from the bullfrog's sacculus. J. Neurosci. 16, 5629–5643 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ricci, A. J., Crawford, A. C. & Fettiplace, R. Active hair bundle motion linked to fast transducer adaptation in auditory hair cells. J. Neurosci. 20, 7131–7142 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Rhode, W. S. Observations of the vibration of the basilar membrane in squirrel monkeys using the Mossbauer technique. J. Acoust. Soc. Am. 49, 1218–1231 (1971).

    Article  Google Scholar 

  68. Emadi, G., Richter, C. P. & Dallos, P. Stiffness of the gerbil basilar membrane: radial and longitudinal variations. J. Neurophysiol. 91, 474–488 (2004).

    Article  PubMed  Google Scholar 

  69. Neely, S. T. & Kim, D. O. An active cochlear model showing sharp tuning and high sensitivity. Hear. Res. 9, 123–130 (1983).

    Article  CAS  PubMed  Google Scholar 

  70. Allen, J. B. & Neely, S. T. Micromechanical models of the cochlea. Phys. Today July, 40–47 (1992).

  71. Brownell, W. E., Bader, C. R., Bertrand, D. & de Ribaupierre, Y. Evoked mechanical responses of isolated cochlear outer hair cells. Science 227, 194–196 (1985).

    Article  CAS  PubMed  Google Scholar 

  72. Ashmore, J. F. A fast motile response in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. J. Physiol. (Lond.) 388, 323–347 (1987). Detailed description of the voltage-dependent somatic contractility of isolated OHCs and evidence for a novel mechanism resident in the cell cortex.

    Article  CAS  Google Scholar 

  73. Zheng, J. et al. Prestin is the motor protein of cochlear outer hair cells. Nature 405, 149–155 (2000). Cloning of prestin by subtractive hybridization of cDNA pools from OHCs relative to IHCs. Showed that prestin bestows voltage-dependent motility when expressed heterologously.

    Article  CAS  PubMed  Google Scholar 

  74. Belyantseva, I. A., Adler, H. J., Curi, R., Frolenkov, G. I. & Kachar, B. Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J. Neurosci. 20, RC116 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Rybalchenko, V. & Santos-Sacchi, J. Cl− flux through a non-selective, stretch-sensitive conductance influences the outer hair cell motor of the guinea pig. J. Physiol. (Lond.) 547, 873–891 (2003).

    Article  CAS  Google Scholar 

  76. Oliver, D. et al. Intracellular anions as the voltage sensor of prestin, the outer hair cell motor protein. Science 292, 2340–2343 (2001).

    Article  CAS  PubMed  Google Scholar 

  77. Liberman, M. C. et al. Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419, 300–304 (2003).

    Article  CAS  Google Scholar 

  78. Cheatham, M. A., Huynh, K. H., Gao, J., Zuo, J. & Dallos, P. Cochlear function in Prestin knockout mice. J. Physiol. (Lond.) 560, 821–830 (2004).

    Article  CAS  Google Scholar 

  79. Santos-Sacchi, J. On the frequency limit and phase of outer hair cell motility. J. Neurosci. 12, 1906–1916 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Housley, G. D. & Ashmore, J. F. Ionic currents of outer hair cells isolated from the guinea-pig cochlea. J. Physiol. (Lond.) 448, 73–98 (1992).

    Article  CAS  Google Scholar 

  81. Frank, G., Hemmert, W. & Gummer, A. W. Limiting dynamics of high-frequency electromechanical transduction of outer hair cells. Proc. Natl Acad. Sci. USA 96, 4420–4425 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Santos-Sacchi, J., Kakehata, S., Kikuchi, T., Katori, Y. & Takasaka, T. Density of motility-related charge in the outer hair cell of the guinea pig is inversely related to best frequency. Neurosci. Lett. 256, 155–158 (1998).

    Article  CAS  PubMed  Google Scholar 

  83. Dallos, P. & Evans, B. N. High frequency outer hair cell motility: corrections and corrigendum. Science 268, 1420–1421 (1995).

    Article  CAS  PubMed  Google Scholar 

  84. Fridberger, A. et al. Organ of Corti potentials and the motion of the basilar membrane. J. Neurosci. 24, 10057–10063 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Russell, I. J. & Kössl, M. The voltage responses of hair cells in the basal turn of the guinea-pig cochlea. J. Physiol. (Lond.) 435, 493–511 (1991).

    Article  CAS  Google Scholar 

  86. Crawford, A. C. & Fettiplace, R. The mechanical properties of ciliary bundles of turtle cochlear hair cells. J. Physiol. (Lond.) 364, 359–379 (1985). Used photodiode imaging to show both active and spontaneous motion of the hair bundle driven by changes in membrane potential

    Article  CAS  Google Scholar 

  87. Hudspeth, A. J. Mechanical amplification of stimuli by hair cells. Curr. Opin. Neurobiol. 7, 480–486 (1997).

    Article  CAS  PubMed  Google Scholar 

  88. Hallworth, R. Passive compliance and active force generation in the guinea pig outer hair cell. J. Neurophysiol. 74, 2319–2328 (1995).

    Article  CAS  PubMed  Google Scholar 

  89. Iwasa, K. H. & Adachi, M. Force generation in the outer hair cell of the cochlea. Biophys. J. 73, 546–555 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Dallos, P. Neurobiology of cochlear inner and outer hair cells: intracellular recordings. Hear. Res. 22, 185–198 (1986).

    Article  CAS  PubMed  Google Scholar 

  91. Adler, H. J. et al. Expression of prestin, a membrane motor protein, in the mammalian auditory and vestibular periphery. Hear. Res. 184, 27–40 (2003).

    Article  CAS  PubMed  Google Scholar 

  92. He, D. Z. et al. Chick hair cells do not exhibit voltage-dependent somatic motility. J. Physiol. (Lond.) 546, 511–520 (2003).

    Article  CAS  Google Scholar 

  93. Kennedy, H. J., Crawford, A. C. & Fettiplace, R. Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 433, 880–883 (2005).

    Article  CAS  PubMed  Google Scholar 

  94. Chan, D. K. & Hudspeth, A. J. Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nature Neurosci. 8, 149–155 (2005). Imaging of IHC bundles in an in vitro cochlear preparation to show mechanical amplification dependent on MET channel function.

    Article  CAS  PubMed  Google Scholar 

  95. Kim, D. O. Active and nonlinear cochlear biomechanics and the role of outer-hair-cell subsystem in the mammalian auditory system. Hear. Res. 22, 105–114 (1986).

    Article  CAS  PubMed  Google Scholar 

  96. Kiang, N. Y., Liberman, M. C., Sewell, W. F. & Guinan, J. J. Single unit clues to cochlear mechanisms. Hear. Res. 22, 171–182 (1986).

    Article  CAS  PubMed  Google Scholar 

  97. Chan, D. K. & Hudspeth, A. J. Mechanical responses of the organ of Corti to acoustic and electrical stimulation in vitro. Biophys. J. 16 Sep 2005 (10.1529/biophysj.105.070474).

  98. He, D. Z., Jia, S. & Dallos, P. Prestin and the dynamic stiffness of cochlear outer hair cells. J. Neurosci. 23, 9089–9096 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Lim, D. J. Cochlear anatomy related to cochlear micromechanics. A review. J. Acoust. Soc. Am. 67, 1686–1695 (1980).

    Article  CAS  PubMed  Google Scholar 

  100. Mammano, F. & Ashmore, J. F. Reverse transduction measured in the isolated cochlea by laser Michelson interferometry. Nature 365, 838–841 (1993).

    Article  CAS  PubMed  Google Scholar 

  101. Russell, I. J. & Sellick, P. M. Intracellular studies of hair cells in the mammalian cochlea. J. Physiol. (Lond.) 284, 261–290 (1978).

    Article  CAS  Google Scholar 

  102. Russell, I. J., Cody, A. R. & Richardson, G. P. The responses of inner and outer hair cells in the basal turn of the guinea-pig cochlea and in the mouse cochlea grown in vitro. Hear. Res. 22, 199–216 (1986).

    Article  CAS  PubMed  Google Scholar 

  103. Eybalin, M. Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol. Rev. 73, 309–373 (1993).

    Article  CAS  PubMed  Google Scholar 

  104. Brown, M. C. & Nuttall, A. L. Efferent control of cochlear inner hair cell responses in the guinea-pig. J. Physiol. (Lond.) 354, 625–646 (1984).

    Article  CAS  Google Scholar 

  105. Atar, O. & Avraham, K. B. Therapeutics of hearing loss: expectations vs reality. Drug Discov. Today 10, 1323–1230 (2005).

    Article  PubMed  Google Scholar 

  106. Marcotti, W., van Netten, S. M. & Kros, C. J. The aminoglycoside antibiotic dihydrostreptomycin rapidly enters mouse outer hair cells through the mechano-electrical transducer channels. J. Physiol. (Lond.) 567, 505–521 (2005).

    Article  CAS  Google Scholar 

  107. Cortopassi, G. & Hutchin, T. A molecular and cellular hypothesis for aminoglycoside-induced deafness. Hear. Res. 78, 27–30 (1994).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by a grant from the National Institute on Deafness and Other Communication Disorders, National Institutes of Health, USA. We thank Y. Katori and D. Furness for the electron micrograph in figure 3b, and C. Dizack for help with the artwork.

Author information

Authors and Affiliations

  1. Department of Physiology, University of Wisconsin Medical School, 185 Medical Sciences Building, 1300 University Avenue, Madison, 53706, Wisconsin, USA

    Robert Fettiplace

  2. MacKay Institute of Communication and Neuroscience, School of Life Sciences, Keele University, Staffordshire, ST5 5BG, UK

    Carole M. Hackney

Authors
  1. Robert Fettiplace
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  2. Carole M. Hackney
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Corresponding author

Correspondence to Robert Fettiplace.

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The authors declare no competing financial interests.

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FURTHER INFORMATION

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Hackney's homepage

Hereditary Hearing Loss Homepage

Glossary

Electromechanical feedback

The electrical change in an OHC caused by basilar membrane vibration generates a movement of the OHC that, in turn, feeds back to or alters basilar membrane vibration.

Reverse transduction

In normal forward transduction, hair cells convert mechanical stimuli into electrical responses. In reverse transduction, the electrical signals of hair cells evoke a mechanical output.

Osmiophilic rootlet

The stem of a stereocilium that in electron micrographs is seen to be heavily stained by osmium, which probably indicates a dense concentration of protein.

Shaker 2 mouse

A congenitally deaf mouse with a mutation in myosin XV that results in abnormally short stereocilia.

PDZ domain

A peptide-binding domain that is important for the organization of membrane proteins, particularly at cell–cell junctions. It can bind to the carboxyl termini of proteins or can form dimers with other PDZ domains. PDZ domains are named after the proteins in which these sequence motifs were originally identified (PSD-95, Discs large, zona occludens 1).

Whirler mouse

A mouse mutant that is unresponsive to sound and shows circling and head-tossing behaviour, indicative of both auditory and vestibular dysfunction. The mutated protein is known as whirlin and is involved in stereocilia elongation.

Usher type I syndrome

One of three subtypes (I,II and III) of hereditary disorder characterized by sensorineural deafness of cochlear origin combined with loss of vision due to retinitis pigmentosa.

Adaptation

The decline in response, and therefore sensitivity, to a sustained stimulus. Adaptation is a property of many sensory receptors that enables them to adjust their sensitivity to prevailing conditions and respond only to changes in stimulus intensity.

Time constant

The time required for the response of a system to decline to 37% of its initial value. For the cell membrane, this is the product of its capacitance and resistance, setting the timescale over which membrane currents change the voltage. A small time constant means that a system's response can change rapidly.

Unitary conductance

The electrical conductance of a single ion channel: the current flowing through the channel divided by the voltage applied across the cell membrane. Unitary conductance is a characteristic channel property but varies according to the ion species present.

Ototoxic agents

Procedures or drugs that damage hearing, primarily by acting on the hair cells.

Varitint-waddler mouse

A mouse with deafness, vestibular and pigmentation defects due to mutation in the mucolipin 3 gene, which encodes the ion channel protein TRPML3. It is associated with progressive hair bundle disorganization and hair cell degeneration.

Photodiode imaging

The stimulator casts a shadow on a pair of photodiodes and, as it moves, the light on one photodiode increases while that on the other decreases. The difference in photocurrents can be used to measure displacements down to a few nanometres.

Low-pass filter

A filter that suppresses all frequencies above a certain point known as the cut-off frequency.

Periodic component

A repetitive waveform: for example, a sine wave.

Compliance

The inverse of stiffness; the displacement of an elastic element produced by a known force.

Sylgard bead

A drop of silicone rubber, a mixture of a base and a curing agent, that is deposited on the tip of a glass fibre while liquid, then polymerized and hardened by heating.

Piezoelectric actuator

A ceramic crystal that deforms when a potential difference is applied across it. Piezoelectric devices require large voltages to induce movements of a micron. Such devices are reversible and also generate a voltage in response to mechanical stress.

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Fettiplace, R., Hackney, C. The sensory and motor roles of auditory hair cells. Nat Rev Neurosci 7, 19–29 (2006). https://doi.org/10.1038/nrn1828

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