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Vol. 68, No. 6, 2006
Issue release date: October 2006
Section title: Cochlear Mechanics and Otoacoustic Emissions
Free Access
ORL 2006;68:373–377
(DOI:10.1159/000095280)

Electromotility in Outer Hair Cells: A Supporting Role for Fast Potassium Conductance

Ospeck M. · Dong X. · Fang J. · Iwasa K.H.
Biophysics Section, NIDCD, NIH, Bethesda, Md., USA
email Corresponding Author

Abstract

Motility of outer hair cells underlies the cochlear amplifier, which is critical for the ear’s sensitivity and fine tuning. Of the two motile mechanisms present in these cells, electromotility at the lateral wall depends on the receptor potential and thus depends on currents through the cell body. We found that, in the guinea pig cochlea, basal turn outer hair cells have a fast-activating ion current (τ < 0.3 ms at 23°C), which is absent in apical turn cells. This finding is consistent with our previous theoretical analysis that a fast-activating potassium current is required only in the basal turn to counteract the capacitive current and thereby to enhance the effectiveness of electromotility. Thus, our finding is consistent with the functional significance of electromotility. We conjecture therefore that the current reduces the capacitance of the outer hair cell in order to increase hearing bandwidth.

© 2006 S. Karger AG, Basel


  

Key Words

  • Outer hair cells
  • Prestin
  • Potassium channel
  • Cochlear amplifier

References

  1. Gold T: Hearing. 2. The physical basis of the action of the cochlea. Proc R Soc Lond B Biol Sci 1948;135:492–498.

    External Resources

  2. Martin P, Hudspeth AJ: Active hair-bundle movements can amplify a hair cell’s response to oscillatory mechanical stimuli. Proc Natl Acad Sci USA 1999;96:14306–14311.
  3. Kennedy HJ, Crawford AC, Fettiplace R: Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 2005;433:880–883.
  4. Brownell W, Bader C, Bertrand D, Ribaupierre Y: Evoked mechanical responses of isolated outer hair cells. Science 1985;227:194–196.
  5. Ashmore JF: A fast motile response in guinea-pig outer hair cells: the molecular basis of the cochlear amplifier. J Physiol 1987;388:323–347.
  6. Santos-Sacchi J, Dilger JP: Whole cell currents and mechanical responses of isolated outer hair cells. Hear Res 1988;65:143–150.

    External Resources

  7. Fettiplace R, Ricci AJ, Hackney CM: Clues to the cochlear amplifier from the turtle ear. Trends Neurosci 2001;24:169–175.
  8. Chan DK, Hudspeth AJ: Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat Neurosci 2005;8:149–155.
  9. Dong XX, Ospeck M, Iwasa KH: Piezoelectric reciprocal relationship of the membrane motor in the cochlear outer hair cell. Biophys J 2002;82:1254–1259.
  10. Zheng J, Shen W, He DZZ, Long KB, Madison LD, Dallos P: Prestin is the motor protein of cochlear outer hair cells. Nature 2000;405:149–155.
  11. Liberman MC, Gao J, He DZ, Wu X, Jia S, Zuo J: Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 2002;419:300–304.
  12. Liberman MC, Zuo J, Guinan JJJ: Otoacoustic emissions without somatic motility: can stereocilia mechanics drive the mammalian cochlea? J Acoust Soc Am 2004;116:1649– 1655.
  13. Hodgkin AL, Huxley AF: A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1955;117:473–496.
  14. Housley GD, Ashmore JF: Ionic currents of outer hair cells isolated from the guinea-pig cochlea. J Physiol 1992;448:73–98.
  15. Mammano F, Ashmore JF: Differential expression of outer hair cell potassium currents in the isolated cochlea of the guinea-pig. J Physiol 1996;496:639–646.
  16. Marcotti W, Kros CJ: Developmental expression of the potassium current IK,n contributes to maturation of mouse outer hair cells. J Physiol 1999;520:653–660.
  17. Kros CJ, Crawford AC: Potassium currents in inner hair cells isolated from the guinea pig cochlea. J Physiol 1990;421:263–291.
  18. Patuzzi R: Cochlear micromechanics and macromechanics; in Dallos P, Popper AN, Fay RR (eds): The Cochlea. New York, Springer, 1996, pp 186–257.
  19. Ospeck M, Dong XX, Iwasa KH: Limiting frequency of the cochlear amplifier based on electromotility of outer hair cells. Biophys J 2003;84:739–749.
  20. Greenwood DD: A cochlear frequency-position function for several species – 29 years later. J Acoust Soc Am 1990;87:2592–1605.
  21. Ashmore JF: Forward and reverse transduction in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. Neurosci Res Suppl 1990;12:S39–S50.
  22. Santos-Sacchi J: Reversible inhibition of voltage-dependent outer hair cell motility and capacitance. J Neurophysiol 1991;11:3096–3110.
  23. Iwasa KH: Effect of stress on the membrane capacitance of the auditory outer hair cell. Biophys J 1993;65:492–498.
  24. Russell IJ, Cody AR, Richardson GP: 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 1986;22:199–216.
  25. Hille B: Ion Channels of Excitable Membranes, ed 3. Sunderland, Sinauer, 2001.
  26. Schuknecht HF: Pathology of the Ear. Philadelphia, Lea & Febiger, 1993.
  27. Ohlemiller KK, Gagnon PM: Cellular correlates of progressive hearing loss in 129S6/SvEv mice. J Comp Neurol 2004;469:377–390.

  

Author Contacts

Kuni Iwasa
Biophysics Section, NIDCD, NIH
50th South Drive MSC 8027
Bethesda, MD 20892-8027 (USA)
Tel. +1 301 496 3987, Fax +1 301 480 0827, E-Mail iwasa@nih.gov

  

Article Information

Published online: October 26, 2006
Number of Print Pages : 5
Number of Figures : 2, Number of Tables : 0, Number of References : 27

  

Publication Details

ORL (Journal for Oto-Rhino-Laryngology and Ist Related Specialties)

Vol. 68, No. 6, Year 2006 (Cover Date: October 2006)

Journal Editor: O'Malley, B.W., Jr. (Philadelphia, Pa.)
ISSN: 0301–1569 (print), 1423–0275 (Online)

For additional information: http://www.karger.com/ORL


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

Abstract

Motility of outer hair cells underlies the cochlear amplifier, which is critical for the ear’s sensitivity and fine tuning. Of the two motile mechanisms present in these cells, electromotility at the lateral wall depends on the receptor potential and thus depends on currents through the cell body. We found that, in the guinea pig cochlea, basal turn outer hair cells have a fast-activating ion current (τ < 0.3 ms at 23°C), which is absent in apical turn cells. This finding is consistent with our previous theoretical analysis that a fast-activating potassium current is required only in the basal turn to counteract the capacitive current and thereby to enhance the effectiveness of electromotility. Thus, our finding is consistent with the functional significance of electromotility. We conjecture therefore that the current reduces the capacitance of the outer hair cell in order to increase hearing bandwidth.

© 2006 S. Karger AG, Basel


  

Author Contacts

Kuni Iwasa
Biophysics Section, NIDCD, NIH
50th South Drive MSC 8027
Bethesda, MD 20892-8027 (USA)
Tel. +1 301 496 3987, Fax +1 301 480 0827, E-Mail iwasa@nih.gov

  

Article Information

Published online: October 26, 2006
Number of Print Pages : 5
Number of Figures : 2, Number of Tables : 0, Number of References : 27

  

Publication Details

ORL (Journal for Oto-Rhino-Laryngology and Ist Related Specialties)

Vol. 68, No. 6, Year 2006 (Cover Date: October 2006)

Journal Editor: O'Malley, B.W., Jr. (Philadelphia, Pa.)
ISSN: 0301–1569 (print), 1423–0275 (Online)

For additional information: http://www.karger.com/ORL


Article / Publication Details

First-Page Preview
Abstract of Cochlear Mechanics and Otoacoustic Emissions

Published online: 10/26/2006
Issue release date: October 2006

Number of Print Pages: 5
Number of Figures: 2
Number of Tables: 0

ISSN: 0301-1569 (Print)
eISSN: 1423-0275 (Online)

For additional information: http://www.karger.com/ORL


Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Gold T: Hearing. 2. The physical basis of the action of the cochlea. Proc R Soc Lond B Biol Sci 1948;135:492–498.

    External Resources

  2. Martin P, Hudspeth AJ: Active hair-bundle movements can amplify a hair cell’s response to oscillatory mechanical stimuli. Proc Natl Acad Sci USA 1999;96:14306–14311.
  3. Kennedy HJ, Crawford AC, Fettiplace R: Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 2005;433:880–883.
  4. Brownell W, Bader C, Bertrand D, Ribaupierre Y: Evoked mechanical responses of isolated outer hair cells. Science 1985;227:194–196.
  5. Ashmore JF: A fast motile response in guinea-pig outer hair cells: the molecular basis of the cochlear amplifier. J Physiol 1987;388:323–347.
  6. Santos-Sacchi J, Dilger JP: Whole cell currents and mechanical responses of isolated outer hair cells. Hear Res 1988;65:143–150.

    External Resources

  7. Fettiplace R, Ricci AJ, Hackney CM: Clues to the cochlear amplifier from the turtle ear. Trends Neurosci 2001;24:169–175.
  8. Chan DK, Hudspeth AJ: Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat Neurosci 2005;8:149–155.
  9. Dong XX, Ospeck M, Iwasa KH: Piezoelectric reciprocal relationship of the membrane motor in the cochlear outer hair cell. Biophys J 2002;82:1254–1259.
  10. Zheng J, Shen W, He DZZ, Long KB, Madison LD, Dallos P: Prestin is the motor protein of cochlear outer hair cells. Nature 2000;405:149–155.
  11. Liberman MC, Gao J, He DZ, Wu X, Jia S, Zuo J: Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 2002;419:300–304.
  12. Liberman MC, Zuo J, Guinan JJJ: Otoacoustic emissions without somatic motility: can stereocilia mechanics drive the mammalian cochlea? J Acoust Soc Am 2004;116:1649– 1655.
  13. Hodgkin AL, Huxley AF: A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1955;117:473–496.
  14. Housley GD, Ashmore JF: Ionic currents of outer hair cells isolated from the guinea-pig cochlea. J Physiol 1992;448:73–98.
  15. Mammano F, Ashmore JF: Differential expression of outer hair cell potassium currents in the isolated cochlea of the guinea-pig. J Physiol 1996;496:639–646.
  16. Marcotti W, Kros CJ: Developmental expression of the potassium current IK,n contributes to maturation of mouse outer hair cells. J Physiol 1999;520:653–660.
  17. Kros CJ, Crawford AC: Potassium currents in inner hair cells isolated from the guinea pig cochlea. J Physiol 1990;421:263–291.
  18. Patuzzi R: Cochlear micromechanics and macromechanics; in Dallos P, Popper AN, Fay RR (eds): The Cochlea. New York, Springer, 1996, pp 186–257.
  19. Ospeck M, Dong XX, Iwasa KH: Limiting frequency of the cochlear amplifier based on electromotility of outer hair cells. Biophys J 2003;84:739–749.
  20. Greenwood DD: A cochlear frequency-position function for several species – 29 years later. J Acoust Soc Am 1990;87:2592–1605.
  21. Ashmore JF: Forward and reverse transduction in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. Neurosci Res Suppl 1990;12:S39–S50.
  22. Santos-Sacchi J: Reversible inhibition of voltage-dependent outer hair cell motility and capacitance. J Neurophysiol 1991;11:3096–3110.
  23. Iwasa KH: Effect of stress on the membrane capacitance of the auditory outer hair cell. Biophys J 1993;65:492–498.
  24. Russell IJ, Cody AR, Richardson GP: 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 1986;22:199–216.
  25. Hille B: Ion Channels of Excitable Membranes, ed 3. Sunderland, Sinauer, 2001.
  26. Schuknecht HF: Pathology of the Ear. Philadelphia, Lea & Febiger, 1993.
  27. Ohlemiller KK, Gagnon PM: Cellular correlates of progressive hearing loss in 129S6/SvEv mice. J Comp Neurol 2004;469:377–390.