Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1993 Nov;65(5):2217–2227. doi: 10.1016/S0006-3495(93)81247-5

Harmonics of outer hair cell motility.

J Santos-Sacchi 1
PMCID: PMC1225953  PMID: 8298045

Abstract

The voltage-dependent mechanical activity of outer hair cells (OHC) from the organ of Corti is considered responsible for the peripheral auditory system's enhanced ability to detect and analyze sound. Nonlinear processes within the inner ear are presumed to be characteristic of this enhancement process. Harmonic distortion in the OHC mechanical response was analyzed under whole-cell voltage clamp. It is shown that the OHC produces DC, fundamental and second harmonic length changes in response to sinusoidal transmembrane voltage stimulation. Mechanical second harmonic distortion decreases with frequency, whereas the predicted transmembrane second harmonic voltage increases with frequency. Furthermore, the phase of the second harmonic distortion does not correspond to the phase of the predicted transmembrane voltage. In contradistinction, it has been previously shown (Santos-Sacchi, J. 1992. Neuroscience. 12:1906-1916) that fundamental voltage and evoked mechanical responses share magnitude and phase characteristics. OHC length changes are modeled as resulting from voltage-dependent cell surface area changes. The model suggests that the observed harmonic responses in the mechanical response are consistent with the nonlinearity of the voltage-to-length change (V-delta L) function. While these conclusions hold for the data obtained with the present voltage clamp protocol and help to understand the mechanism of OHC motility, modeling the electromechanical system of the OHC in the in vivo state indicates that the mechanical nonlinearity of the OHC contributes minimally to mechanical distortion. That is, in vivo, at moderate sound pressure levels and below, the dominant factor which contributes to nonlinearities of the OHC mechanical response resides within the nonlinear, voltage-generating, stereociliar transduction process.

Full text

PDF
2217

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ashmore J. F. A fast motile response in guinea-pig outer hair cells: the cellular basis of the cochlear amplifier. J Physiol. 1987 Jul;388:323–347. doi: 10.1113/jphysiol.1987.sp016617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ashmore J. F., Meech R. W. Ionic basis of membrane potential in outer hair cells of guinea pig cochlea. Nature. 1986 Jul 24;322(6077):368–371. doi: 10.1038/322368a0. [DOI] [PubMed] [Google Scholar]
  3. Brownell W. E. Outer hair cell electromotility and otoacoustic emissions. Ear Hear. 1990 Apr;11(2):82–92. doi: 10.1097/00003446-199004000-00003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dallos P., Evans B. N., Hallworth R. Nature of the motor element in electrokinetic shape changes of cochlear outer hair cells. Nature. 1991 Mar 14;350(6314):155–157. doi: 10.1038/350155a0. [DOI] [PubMed] [Google Scholar]
  5. Dallos P. Neurobiology of cochlear inner and outer hair cells: intracellular recordings. Hear Res. 1986;22:185–198. doi: 10.1016/0378-5955(86)90095-x. [DOI] [PubMed] [Google Scholar]
  6. Dallos P., Santos-Sacchi J., Flock A. Intracellular recordings from cochlear outer hair cells. Science. 1982 Nov 5;218(4572):582–584. doi: 10.1126/science.7123260. [DOI] [PubMed] [Google Scholar]
  7. Dallos P. The active cochlea. J Neurosci. 1992 Dec;12(12):4575–4585. doi: 10.1523/JNEUROSCI.12-12-04575.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Evans B. N., Hallworth R., Dallos P. Outer hair cell electromotility: the sensitivity and vulnerability of the DC component. Hear Res. 1991 Apr;52(2):288–304. doi: 10.1016/0378-5955(91)90019-6. [DOI] [PubMed] [Google Scholar]
  9. Forge A. Structural features of the lateral walls in mammalian cochlear outer hair cells. Cell Tissue Res. 1991 Sep;265(3):473–483. doi: 10.1007/BF00340870. [DOI] [PubMed] [Google Scholar]
  10. Gulley R. L., Reese T. S. Regional specialization of the hair cell plasmalemma in the organ of corti. Anat Rec. 1977 Sep;189(1):109–123. doi: 10.1002/ar.1091890108. [DOI] [PubMed] [Google Scholar]
  11. Holley M. C., Ashmore J. F. A cytoskeletal spring in cochlear outer hair cells. Nature. 1988 Oct 13;335(6191):635–637. doi: 10.1038/335635a0. [DOI] [PubMed] [Google Scholar]
  12. Holley M. C., Ashmore J. F. On the mechanism of a high-frequency force generator in outer hair cells isolated from the guinea pig cochlea. Proc R Soc Lond B Biol Sci. 1988 Jan 22;232(1269):413–429. doi: 10.1098/rspb.1988.0004. [DOI] [PubMed] [Google Scholar]
  13. Holley M. C., Kalinec F., Kachar B. Structure of the cortical cytoskeleton in mammalian outer hair cells. J Cell Sci. 1992 Jul;102(Pt 3):569–580. doi: 10.1242/jcs.102.3.569. [DOI] [PubMed] [Google Scholar]
  14. Housley G. D., Ashmore J. F. Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc Biol Sci. 1991 May 22;244(1310):161–167. doi: 10.1098/rspb.1991.0065. [DOI] [PubMed] [Google Scholar]
  15. Housley G. D., Ashmore J. F. Ionic currents of outer hair cells isolated from the guinea-pig cochlea. J Physiol. 1992 Mar;448:73–98. doi: 10.1113/jphysiol.1992.sp019030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Iwasa K. H., Chadwick R. S. Elasticity and active force generation of cochlear outer hair cells. J Acoust Soc Am. 1992 Dec;92(6):3169–3173. doi: 10.1121/1.404194. [DOI] [PubMed] [Google Scholar]
  17. Iwasa K. H. Effect of stress on the membrane capacitance of the auditory outer hair cell. Biophys J. 1993 Jul;65(1):492–498. doi: 10.1016/S0006-3495(93)81053-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kalinec F., Holley M. C., Iwasa K. H., Lim D. J., Kachar B. A membrane-based force generation mechanism in auditory sensory cells. Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8671–8675. doi: 10.1073/pnas.89.18.8671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kros C. J., Rüsch A., Richardson G. P. Mechano-electrical transducer currents in hair cells of the cultured neonatal mouse cochlea. Proc Biol Sci. 1992 Aug 22;249(1325):185–193. doi: 10.1098/rspb.1992.0102. [DOI] [PubMed] [Google Scholar]
  20. Nakagawa T., Kakehata S., Akaike N., Komune S., Takasaka T., Uemura T. Calcium channel in isolated outer hair cells of guinea pig cochlea. Neurosci Lett. 1991 Apr 15;125(1):81–84. doi: 10.1016/0304-3940(91)90136-h. [DOI] [PubMed] [Google Scholar]
  21. Patuzzi R. B., Yates G. K., Johnstone B. M. Outer hair cell receptor current and sensorineural hearing loss. Hear Res. 1989 Oct;42(1):47–72. doi: 10.1016/0378-5955(89)90117-2. [DOI] [PubMed] [Google Scholar]
  22. Ruggero M. A. Responses to sound of the basilar membrane of the mammalian cochlea. Curr Opin Neurobiol. 1992 Aug;2(4):449–456. doi: 10.1016/0959-4388(92)90179-o. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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. 1986;22:199–216. doi: 10.1016/0378-5955(86)90096-1. [DOI] [PubMed] [Google Scholar]
  24. Saito K. Fine structure of the sensory epithelium of guinea-pig organ of Corti: subsurface cisternae and lamellar bodies in the outer hair cells. Cell Tissue Res. 1983;229(3):467–481. doi: 10.1007/BF00207692. [DOI] [PubMed] [Google Scholar]
  25. Santos-Sacchi J. Asymmetry in voltage-dependent movements of isolated outer hair cells from the organ of Corti. J Neurosci. 1989 Aug;9(8):2954–2962. doi: 10.1523/JNEUROSCI.09-08-02954.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Santos-Sacchi J., Dilger J. P. Whole cell currents and mechanical responses of isolated outer hair cells. Hear Res. 1988 Sep 15;35(2-3):143–150. doi: 10.1016/0378-5955(88)90113-x. [DOI] [PubMed] [Google Scholar]
  27. Santos-Sacchi J. On the frequency limit and phase of outer hair cell motility: effects of the membrane filter. J Neurosci. 1992 May;12(5):1906–1916. doi: 10.1523/JNEUROSCI.12-05-01906.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Santos-Sacchi J. Reversible inhibition of voltage-dependent outer hair cell motility and capacitance. J Neurosci. 1991 Oct;11(10):3096–3110. doi: 10.1523/JNEUROSCI.11-10-03096.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES