Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

A differentially amplified motion in the ear for near-threshold sound detection

Nature Neuroscience volume 14, pages 770–774 (2011)Cite this article

Subjects

Abstract

The ear is a remarkably sensitive pressure fluctuation detector. In guinea pigs, behavioral measurements indicate a minimum detectable sound pressure of ∼20 μPa at 16 kHz. Such faint sounds produce 0.1-nm basilar membrane displacements, a distance smaller than conformational transitions in ion channels. It seems that noise within the auditory system would swamp such tiny motions, making weak sounds imperceptible. Here we propose a new mechanism contributing to a resolution of this problem and validate it through direct measurement. We hypothesized that vibration at the apical side of hair cells is enhanced compared with that at the commonly measured basilar membrane side. Using in vivo optical coherence tomography, we demonstrated that apical-side vibrations peaked at a higher frequency, had different timing and were enhanced compared with those at the basilar membrane. These effects depend nonlinearly on the stimulus sound pressure level. The timing difference and enhancement of vibrations are important for explaining how the noise problem is circumvented.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The cochlea and organ of Corti.
Figure 2: Vibration in the organ of Corti of a guinea pig cochlea.
Figure 3: Displacement magnitude as a function of sound level (input–output function) measured from the basilar membrane and reticular lamina.
Figure 4: Sound-induced vibration of the basilar membrane and reticular lamina at the cochlear location giving a maximal vibration response at 19 kHz (BF) in a guinea pig with 7 dB sensitivity loss owing to surgical preparation.
Figure 5: Phase differences of reticular lamina displacement and organ of Corti receptor potential compared with basilar membrane motion.

Similar content being viewed by others

References

  1. Heffner, R., Heffner, H. & Masterton, B. Behavioral measurements of absolute and frequency-difference thresholds in guinea pig. J. Acoust. Soc. Am. 49, 1888–1895 (1971).

    Article  CAS  Google Scholar 

  2. Prosen, C.A., Petersen, M.R., Moody, D.B. & Stebbins, W.C. Auditory thresholds and kanamycin-induced hearing loss in the guinea pig assessed by a positive reinforcement procedure. J. Acoust. Soc. Am. 63, 559–566 (1978).

    Article  CAS  Google Scholar 

  3. Hood, L.J. et al. Objective auditory threshold estimation using sine-wave derived responses. Hear. Res. 55, 109–116 (1991).

    Article  CAS  Google Scholar 

  4. Cooper, N.P. & Guinan, J.J. Jr. Efferent-mediated control of basilar membrane motion. J. Physiol. (Lond.) 576, 49–54 (2006).

    Article  CAS  Google Scholar 

  5. Khanna, S.M. & Leonard, D.G.B. Basilar membrane tuning in the cat cochlea. Science 215, 305–306 (1982).

    Article  CAS  Google Scholar 

  6. Sellick, P.M., Patuzzi, R. & Johnstone, B.M. Measurement of basilar membrane motion in the guinea pig using Mössbauer technique. J. Acoust. Soc. Am. 72, 131–141 (1982).

    Article  CAS  Google Scholar 

  7. Fridberger, A., Tomo, I., Ulfendahl, M. & Boutet de Monvel, J. Imaging hair cell transduction at the speed of sound: dynamic behavior of mammalian stereocilia. Proc. Natl. Acad. Sci. USA 103, 1918–1923 (2006).

    Article  CAS  Google Scholar 

  8. 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  Google Scholar 

  9. van Netten, S.M., Dinklo, T., Marcotti, W. & Kros, C.J. Channel gating forces govern accuracy of mechano-electrical transduction in hair cells. Proc. Natl. Acad. Sci. USA 100, 15510–15515 (2003).

    Article  CAS  Google Scholar 

  10. Denk, W. & Webb, W.W. Thermal-noise-limited transduction observed in mechanosensory receptors of the inner ear. Phys. Rev. Lett. 63, 207–210 (1989).

    Article  CAS  Google Scholar 

  11. Bialek, W. Physical limits to sensation and perception. Annu. Rev. Biophys. Biophys. Chem. 16, 455–478 (1987).

    Article  CAS  Google Scholar 

  12. Pickles, J.O. An Introduction to the Physiology of Hearing 2nd edn. (Emerald Group, West Yorkshire, 1988).

  13. Barral, J., Dierkes, K., Lindner, B., Jülicher, F. & Martin, P. Coupling a sensory hair-cell bundle to cyber clones enhances nonlinear amplification. Proc. Natl. Acad. Sci. USA 107, 8079–8084 (2010).

    Article  CAS  Google Scholar 

  14. Robles, L. & Ruggero, M.A. Mechanics of the mammalian cochlea. Physiol. Rev. 81, 1305–1352 (2001).

    Article  CAS  Google Scholar 

  15. Kolston, P.J. Comparing in vitro, in situ, and in vivo experimental data in a three-dimensional model of mammalian cochlear mechanics. Proc. Natl Acad. Sci. USA 96, 3676–3681 (1999).

    Article  CAS  Google Scholar 

  16. Olson, E.S. & Mountain, D.C. In vivo measurement of basilar membrane stiffness. J. Acoust. Soc. Am. 89, 1262–1275 (1991).

    Article  CAS  Google Scholar 

  17. Flock, Å. Transducing mechanisms in the lateral line canal organ receptors. Cold Spring Harb. Symp. Quant. Biol. 30, 133–145 (1965).

    Article  CAS  Google Scholar 

  18. Hudspeth, A.J. & Corey, D.P. Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. Proc. Natl. Acad. Sci. USA 74, 2407–2411 (1977).

    Article  CAS  Google Scholar 

  19. Corey, D.P. & Hudspeth, A.J. Ionic basis of the receptor potential in a vertebrate hair cell. Nature 281, 675–677 (1979).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Choudhury, N. et al. Low coherence interferometry of the cochlear partition. Hear. Res. 220, 1–9 (2006).

    Article  Google Scholar 

  22. Chen, F. et al. In vivo imaging and low-coherence interferometry of organ of Corti vibration. J. Biomed. Opt. 12, 021006 (2007).

    Article  Google Scholar 

  23. Rhode, W.S. Observations of the vibration of the basilar membrane in squirrel monkeys using the Mössbauer technique. J. Acoust. Soc. Am. 49 (suppl. 2): 1218–1231 (1971).

    Article  Google Scholar 

  24. Nuttall, A.L., Dolan, D.F. & Avinash, G. Laser Doppler velocimetry of basilar membrane vibration. Hear. Res. 51, 203–213 (1991).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  26. 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  Google Scholar 

  27. 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  Google Scholar 

  28. Nuttall, A.L. & Ren, T. Electromotile hearing: evidence from basilar membrane motion and otoacoustic emissions. Hear. Res. 92, 170–177 (1995).

    Article  CAS  Google Scholar 

  29. Zheng, J. et al. Prestin is the motor protein of cochlear outer hair cells. Nature 405, 149–155 (2000).

    Article  CAS  Google Scholar 

  30. Chan, D.K. & Hudspeth, A.J. Ca2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat. Neurosci. 8, 149–155 (2005).

    Article  CAS  Google Scholar 

  31. 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  Google Scholar 

  32. Denk, W. & Webb, W.W. Forward and reverse transduction at the limit of sensitivity studied by correlating electrical and mechanical fluctuations in frog saccular hair cells. Hear. Res. 60, 89–102 (1992).

    Article  CAS  Google Scholar 

  33. Jaramillo, F. & Wiesenfeld, K. Mechanoelectrical transduction assisted by Brownian motion: a role for noise in the auditory system. Nat. Neurosci. 1, 384–388 (1998).

    Article  CAS  Google Scholar 

  34. Ruggero, M.A. & Temchin, A.N. Unexceptional sharpness of frequency tuning in the human cochlea. Proc. Natl. Acad. Sci. USA 102, 18614–18619 (2005).

    Article  CAS  Google Scholar 

  35. de Boer, E. & Nuttall, A.L. The mechanical waveform of the basilar membrane. III. Intensity effects. J. Acoust. Soc. Am. 107, 1497–1507 (2000).

    Article  CAS  Google Scholar 

  36. Allen, J.B. Cochlear micromechanics—a physical model of tranduction. J. Acoust. Soc. Am. 68, 1660–1670 (1980).

    Article  CAS  Google Scholar 

  37. Gummer, A.W., Hemmert, W. & Zenner, H.-P. Resonant tectorial membrane motion in the inner ear: its crucial role in frequency tuning. Proc. Natl. Acad. Sci. USA 93, 8727–8732 (1996).

    Article  CAS  Google Scholar 

  38. Zwislocki, J.J. & Kletsky, E.J. Tectorial membrane: a possible effect on frequency analysis in the cochlea. Science 204, 639–641 (1979).

    Article  CAS  Google Scholar 

  39. Dallos, P. in Biophysics of the Cochlea: Molecules to Models (ed. Gummer, A.W.) 97–109 (World Scientific, Titisee, Germany, 2002).

  40. Ruggero, M.A. & Rich, N.C. Furosemide alters organ of corti mechanics: evidence for feedback of outer hair cells upon the basilar membrane. J. Neurosci. 11, 1057–1067 (1991).

    Article  CAS  Google Scholar 

  41. Narayan, S.S., Temchin, A.N., Recio, A. & Ruggero, M.A. Frequency tuning of basilar membrane and auditory nerve fibers in the same cochleae. Science 282, 1882–1884 (1998).

    Article  CAS  Google Scholar 

  42. Fridberger, A. & de Monvel, J.B. Sound-induced differential motion within the hearing organ. Nat. Neurosci. 6, 446–448 (2003).

    Article  CAS  Google Scholar 

  43. Tomo, I., Boutet de Monvel, J. & Fridberger, A. Sound-evoked radial strain in the hearing organ. Biophys. J. 93, 3279–3284 (2007).

    Article  CAS  Google Scholar 

  44. Khanna, S.M. & Hao, L.F. Amplification in the apical turn of the cochlea with negative feedback. Hear. Res. 149, 55–76 (2000).

    Article  CAS  Google Scholar 

  45. Baden-Kristensen, K. & Weiss, T.F. Receptor potentials of lizard hair cells with free-standing stereocilia: responses to acoustic clicks. J. Physiol. 335, 699–721 (1983).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank E. de Boer, T. Ren, A. Magnusson and P. Gillespie for critical discussions and reading of the manuscript. This work was supported by US National Institutes of Health, National Institute on Deafness and Other Communication Disorders grants DC00141 (A.L.N.), DC010399 (A.L.N.) and DC010201 (R.K.W.); and Swedish Research Council grant K2008-63X-14061-08-3, the Tysta Skolan Foundation and Hörselskadades Riksförbund (A.F.).

Author information

Author notes

  1. Fangyi Chen, Dingjun Zha, Anders Fridberger and Jiefu Zheng: These authors contributed equally to this work.

Authors and Affiliations

  1. Oregon Hearing Research Center, Oregon Health & Science University, Portland, Oregon, USA

    Fangyi Chen, Dingjun Zha, Anders Fridberger, Jiefu Zheng, Xiaorui Shi & Alfred L Nuttall

  2. Department of Otolaryngology/Head & Neck Surgery, Xijing Hospital, Fourth Military Medical University, China

    Dingjun Zha

  3. Department of Clinical Science, Center for Hearing and Communication Research, Intervention and Technology, Karolinska Institutet, Stockholm, Sweden

    Anders Fridberger

  4. Department of Biomedical Engineering, Oregon Health & Science University, Portland, Oregon, USA

    Niloy Choudhury, Steven L Jacques & Alfred L Nuttall

  5. Department of Dermatology, Oregon Health & Science University, Portland, Oregon, USA

    Steven L Jacques

  6. Department of Bioengineering, University of Washington, Seattle, Washington, USA

    Ruikang K Wang

  7. The Institute of Microcirculation, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China

    Xiaorui Shi

  8. Kresge Hearing Research Institute, The University of Michigan, Michigan, Ann Arbor, USA

    Alfred L Nuttall

Authors
  1. Fangyi Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dingjun Zha
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anders Fridberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiefu Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Niloy Choudhury
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Steven L Jacques
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ruikang K Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaorui Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alfred L Nuttall
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

F.C., D.Z., A.F., J.Z. and N.C. conducted experiments. F.C., D.Z., A.F., J.Z., X.S. and A.L.N. analyzed and interpreted data. F.C., A.F., J.Z. and A.L.N. wrote the manuscript. F.C., N.C., S.L.J. and R.K.W. designed and built the OCT interferometer. F.C., A.F., J.Z. and A.L.N. designed the experiments. F.C., D.Z., A.F. and J.Z. contributed equally.

Corresponding author

Correspondence to Alfred L Nuttall.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, F., Zha, D., Fridberger, A. et al. A differentially amplified motion in the ear for near-threshold sound detection. Nat Neurosci 14, 770–774 (2011). https://doi.org/10.1038/nn.2827

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2827

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing