Skip to main content

Advertisement

Log in

Mechanosensitive Channels in the Lateral Wall Can Enhance the Cochlear Outer Hair Cell Frequency Response

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

We present the results of a modeling study on the impact of mechanosensitive channels in the lateral wall of the outer hair cell on the cell frequency response. The model includes the electrical properties of the cell membrane, piezoelectricity associated with a membrane motor mechanism, and mechanosensitive channels in the cell lateral wall. The outer hair cell is loaded by the vibrating basilar and tectorial membranes, and this loading generates strain in the lateral wall. Our analysis reveals a property, the strain rate sensitivity, that, in concert with the piezoelectric effect, can enhance the cell frequency response. We discuss possible viscoelastic-type mechanisms of the channel’s strain rate sensitivity that is consistent with the organization of the composite cell lateral wall. The parameters of our model are chosen on the basis of the previously estimated electrical and piezoelectric properties as well as typical conductance and density of the mechanosensitive channels in cells. We found that the strain rate sensitivity of the channels can result in receptor potentials greater than those predicted by the RC (resistance and capacitance) analysis. The effect of the channels is especially significant in an intermediate range of sound frequencies, and the channel-related gain is up to 3–4 times between 3 and 15 kHz.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Bett, G. C. L., and F. Sachs. Activation and inactivation of mechanosensitive channels in the chick heart. J. Membr. Biol. 173:237–254, 2000.

    Article  PubMed  Google Scholar 

  2. Brownell, W. E., C. R. Bader, D. Bertrand, and Y. de Ribaupierre. Evoked mechanical responses of isolated cochlear outer hair cell. Science 227:194–196, 1985.

    PubMed  Google Scholar 

  3. Brownell, W. E., A. A. Spector, R. M. Raphael, and A. S. Popel. Micro- and nanomechanics of the cochlear outer hair cell. Annu. Rev. Biomed. Eng. 3:169–194, 2001.

    Article  PubMed  Google Scholar 

  4. Choe, Y., M. O. Magnasco, and A. J. Hudspeth. A model for amplification of hair-bundle motion by cyclical binding of Ca2+ to mechanoelectrical-transduction channels. Proc Natl Acad Sci USA 95:15321–15326, 1998.

    Article  PubMed  Google Scholar 

  5. Corey D. P., and A. J. Hudspeth. Response latency of vertebrate hair cells. Biophys. J. 26:499–506, 1979.

    PubMed  Google Scholar 

  6. Dallos, P. Overview: Cochlear neurobiology. In: The Cochlea, edited by P. Dallos, A. N. Popper, and R. R. Fay. New York: Springer-Verlag, 1996, pp. 1–43.

    Google Scholar 

  7. Dallos, P., and B. N. Evans. High-frequency motility of outer hair cells and the cochlear amplifier. Science 267:2006–2009, 1995.

    PubMed  Google Scholar 

  8. Ding, J. P., R. P. Salvi, and F. Sachs. Stretch-activated channels in guinea pig outer hair cell. Hear. Res. 56:19–28, 1991.

    Article  PubMed  Google Scholar 

  9. Evans, E., and R. Skalak. Mechanics and Thermodynamics of Biomembranes. Boca Raton: CRC Press, 1980, 254 pp.

    Google Scholar 

  10. Fabry, B., G. N. Maksym, J. P. Butler, M. Glogauer, D. Navajas, and J. J. Fredberg. Scaling the microreology of living cells. Phys. Rev. Lett. 87:148102 (1–4), 2001.

    Article  Google Scholar 

  11. Frank, G., W. Hemmer, and A. W. Gummer. Limiting dynamics of high-frequency electromechanical transduction of outer hair cells. Proc. Natl. Acad. Sci. USA. 96:4420–4425, 1999.

    Article  PubMed  Google Scholar 

  12. Geisler, C. D. From Sound to Synapse. New York: Oxford University Press, 1998, 381 pp.

    Google Scholar 

  13. Geleoc, G. S.G, G. W. T. Lennan, G. P. Richardson, and C. R. Kros. 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 

  14. Hamill, O. P., and B. Martinac. Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81:685–739, 2001.

    PubMed  Google Scholar 

  15. Housley, G. D. and J. F. Ashmore. Ionic currents of outer hair cells isolated from guinea-pig cochlea. J. Physiol. 448:73–98, 1992.

    PubMed  Google Scholar 

  16. Iwasa, K. H., M. Li, M. Jia, and B. Kachar. Stretch sensitivity of the lateral wall of the auditory outer hair cell from the guinea pig. Nuerosci. Lett. 133:171–174, 1991.

    Article  Google Scholar 

  17. Kros, C. J., A. Rusch, and G. P. Richardson. Mechanoelectrical transducer currents in hair cells of cultured neonatal mouse cochlea. Proc. R. Soc. Lond. B 249:185–193, 1992.

    Google Scholar 

  18. Kros, C. J. Physiology of mammalian cochlear hair cells. In: The Cochlea, edited by P. Dallos, A. N. Popper, and R. R. Fay. New York: Springer-Verlag, 1996, pp. 318–385.

    Google Scholar 

  19. Liberman, M. C., J. Gao, D. Z.-Z. He, X. Wu, S. Jia, and J. Zuo. Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300–304, 2002.

    Article  PubMed  Google Scholar 

  20. Mammano, F., and J. F. Ashmore. Reverse transduction measured in the isolated cochlea by laser Michelson interferometry. Nature 365:838–841, 1993

    Article  PubMed  Google Scholar 

  21. Mammano, F., and J. F. Ashmore. Differential expression of outer hair cell potassium currents in the isolated cochlea of the guinea-pig. J. Physiol. 496:639–646, 1996.

    PubMed  Google Scholar 

  22. Markin, V. S., and A. J. Hudspeth. Gating-spring models of mechanoelectrical transduction by hair cells of the internal ear. Annu. Rev. Biophys. Biomol. Struct. 24:59–83, 1995.

    Article  PubMed  Google Scholar 

  23. McBride, D. W., and O. P. Hamill. Presure-clamp technique for measurement of the relaxation kinetics of mechanosensitive channels. Trends Neurosci. 16:341–345, 1993.

    Article  PubMed  Google Scholar 

  24. Morimoto, N., R. M. Raphael, A. Nygren, and W. E. Brownell. Excess plasma membrane and effects of ionic amphipaths on mechanics of outer hair cell lateral wall. Am. J. Physiol. Cell Physiol. 282:C1076–1086, 2002.

    Google Scholar 

  25. Morris, C. E. Mechanosensitive ion channels in eukaryotic cells. In: Cell Physiology. Source Book (second edition), edited by N. Sperelakis. San Diego: Academic Press, 1997, pp. 668–681.

    Google Scholar 

  26. Oliver, D., D. Z.-Z. He, N. Klocker, J. Ludwig, U. Schulte, S. Waldegger, J. P. Ruppersberg, P. Dallos, and B. Fakler. Intracellular anions as the voltage-sensor of Prestin, the outer hair cell motor protein. Science 292:2340–2343, 2001.

    Article  PubMed  Google Scholar 

  27. Ospeck, M., X.-X. Dong, and K. H. Iwasa. Limiting frequency of the cochlear amplifier based on electromotility of outer hair cell. Biophys. J. 84:739–749, 2003.

    PubMed  Google Scholar 

  28. Ruggero, M. A. Responses to sound of the basilar membrane of the mammalian cochlea. Curr. Opin. Neurobiol. 2:449–456, 1992.

    Article  PubMed  Google Scholar 

  29. Russell, I. J., and K. E. Nilsen. The location of the cochlear amplifier: Spatial representationof a single tone of the guinea pig basilar membrane. Proc. Natl. Acad. Sci. USA. 94:2660–2664, 1997.

    Article  PubMed  Google Scholar 

  30. Rybalchenko, V., and J. Santos-Sacchi. Cl- flux through a non-selective, stretch-sensitive conductance influences the outer hair cell motor of the guinea-pig. J. Physiol. 547:873–891, 2003.

    Article  PubMed  Google Scholar 

  31. Sachs, F., and C. Morris. Mechanosensitive ion channels in non-specialized cells. In: Reviews of Physiology Biochemistry and Pharmacology, edited by M. P. Blaustein. Berlin: Springer-Verlag, 1998, pp. 1–78.

    Google Scholar 

  32. Santos-Sacchi, J. On the frequency limit and phase of outer hair cell motility: Effects of the membrane filter. J. Neurosci. 12:1906–1916, 1992.

    PubMed  Google Scholar 

  33. Santos-Sacchi J, G. J. Huang, and M. Wu. Mapping the distribution of outer hair cell voltage-dependent conductances by electrical amputation. Biophys. J. 73:1424–1429, 1997.

    PubMed  Google Scholar 

  34. Santos-Sacchi, J., S. Kakehata, T. Kikuchi, Y. Katory, and T. Takasaka. 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  PubMed  Google Scholar 

  35. Sato, M, D. P. Theret, L. T. Wheeler, N. Oshima, and R. M. Nerem. Application of the micropipette technique to the measurement of cultured porcine aortic endothelial cell viscoelastic properties. J. Biomech. Eng. 112:263–268, 1990.

    PubMed  Google Scholar 

  36. Sit, P. S., A. A. Spector, A. J. Lue, A. S. Popel, and W. E. Brownell. Micropipette aspiration on the outer hair cell lateral wall. Biophys. J. 72:2812–2819, 1997.

    PubMed  Google Scholar 

  37. Spector, A. A., M. Ameen, R. A. Schmiedt. Modeling 3-D deformation of outer hair cells and their production of the active force in the cochlea. Biomech. Model. Mechanobiol. 1:123–135, 2002.

    Article  PubMed  Google Scholar 

  38. Spector, A. A., W. E. Brownell, and A. S. Popel. Effect of the membrane piezoelectric properties on the outer hair cell receptor potential under high-frequency conditions. In: Abstracts of the 29th Meeting of ARO, January, 2002, St. Petersburg Beach, Florida, 2002, p. 255.

  39. Spector, A. A., W. E. Brownell, and A. S. Popel. Effect of outer hair cell piezoelectricity on high-frequency receptor potentials. J. Acoust. Soc. Am. 113:453–461, 2003.

    Article  PubMed  Google Scholar 

  40. Steele, C. R., G. Baker, J. A. Tolomeo, and D. Zetes. Electromechanical models of outer hair cell. In: Biophysics of Hair Cell Sensory Systems, edited by H. Duifhuis, J. W. Horst, P. van Dijk, and S. M. van Netten. Singapore: World Scientific Press, 1993, pp. 207–214.

    Google Scholar 

  41. Tolomeo, J. A., and C. R. Steele. Orthotropic piezoelectric properties of cochlear outer hair cell wall. J. Acoust. Soc. Am. 97:3006–3011, 1995.

    Article  PubMed  Google Scholar 

  42. Wang, N. Mechanical interaction among cytoskeletal filaments. Hypertension 32:162–165, 1998.

    PubMed  Google Scholar 

  43. Wang, N., and D. E. Ingber. Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66:2181–2189, 1994.

    PubMed  Google Scholar 

  44. Weitzel, E. K., R. Tasker, and W. E. Brownell. Outer hair cell piezoelectricity: Frequency response enhancement and resonance behavior. J. Acoust. Soc. Am. 114:1462–1466, 2003.

    Article  PubMed  Google Scholar 

  45. Zheng, J., W. Shen, D. Z.-Z. He, K. B. Long, L. D. Madison, and P. Dallos. Prestin is the motor protein of cochlear outer hair cell. Nature 405:149–155, 2000.

    Article  PubMed  Google Scholar 

  46. Zwislocki, J. J. Auditory Sound Transmission. Mahwah, NJ: Lawrence Erlbaum Associates, 2002, 419 pp.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander A. Spector.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Spector, A.A., Popel, A.S., Eatock, R.A. et al. Mechanosensitive Channels in the Lateral Wall Can Enhance the Cochlear Outer Hair Cell Frequency Response. Ann Biomed Eng 33, 991–1002 (2005). https://doi.org/10.1007/s10439-005-5749-0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-005-5749-0

Keywords

Navigation