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Mechanoelectrical transduction assisted by Brownian motion: a role for noise in the auditory system

Nature Neuroscience volume 1, pages 384–388 (1998)Cite this article

Abstract

The organs of the vestibular, auditory and lateral line systems rely on a common strategy for the stimulation of their primary receptors, the hair cells: stimuli induce shear between hair cell epithelia and accessory structures to which hair bundles, the hair cells' mechanosensitive organelles, are attached. The inner hair cells of the cochlea, whose hair bundles are not attached to the overlying tectorial membrane, are a notable exception. Because their hair bundles are not restrained, they undergo significant Brownian motion, a characteristic traditionally thought to blunt the sensitivity of hearing. Contrary to this view, the work reported here indicates that Brownian motion of the hair bundle serves to enhance the sensitivity of mechanoelectrical transduction.

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Figure 1: Control of the stimulus probe.
Figure 2: Spectral density of mechanoelectrical transduction at different noise levels.
Figure 3: Noise dependence of SNRs for mechanoelectrical transduction.

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References

  1. de Vries, H. L. Brownian movement and hearing. Physica 14, 48–60 (1948).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Harris, G. G. Brownian motion in the cochlear partition. J. Acoust. Soc. Am. 44, 176–186 ( 1968).

    Article  CAS  Google Scholar 

  4. Wiesenfeld, K. & Moss, F. Stochastic resonance and the benefits of noise: from ice ages to crayfish and SQUIDs. Nature 373, 33–36 (1995).

    Article  CAS  Google Scholar 

  5. McNamara, B. & Wiesenfeld, K. Theory of stochastic resonance. Phys. Rev. A 39, 4854– 4869 (1989).

    Article  CAS  Google Scholar 

  6. Bezrukov, S. M. & Vodyanov, I. Noise-induced enhancement of signal transduction across voltage-dependent ion channels. Nature 378, 362–364 (1995).

    Article  CAS  Google Scholar 

  7. Collins, J. J., Imhoff, T. T. & Grigg, P. Noise-enhanced information transmission in rat SA1 cutaneous mechanoreceptors via aperiodic stochastic resonance. J. Neurophysiol. 76, 642–645 ( 1996).

    Article  CAS  Google Scholar 

  8. Levin, J. E. & Miller, J. P. Broadband neural encoding in the cricket cercal sensory system enhanced by stochastic resonance. Nature 380, 165–168 ( 1996).

    Article  CAS  Google Scholar 

  9. Douglass, J. K., Wilkens, L., Pantazelou, E. & Moss, F. Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365, 337– 340 (1993).

    Article  CAS  Google Scholar 

  10. Narins, P. M., Benedix, J. H. Jr., & Moss, F. Can increasing temperature improve information transfer in the anuran peripheral auditory system? Aud. Neurosci. 3, 389–400 (1997).

    Google Scholar 

  11. Svrcek-Seiler, W. A., Gebeshuber, I. C., Rattay, F., Biro, T. S. & Markum, H. Micromechanical models for the Brownian motion of hair cell stereocilia. J. Theor. Biol. (in press).

  12. Lindeman, H. H., Ades, H. W., Bredberg, G. & Engström, H. The sensory hairs and the tectorial membrane in the development of the cat's organ of Corti. Acta Otolaryngol. 72, 229 –242 (1972).

    Article  Google Scholar 

  13. Dallos, P. Response characteristics of mammalian cochlear hair cells. J. Neurosci. 5, 1591–1608 ( 1985).

    Article  CAS  Google Scholar 

  14. Dallos, P., Billone, M. C., Durrant, J. D., Wang, C. & Raynor, S. Cochlear inner and outer hair cells: functional differences. Science 177, 356 –358 (1985).

    Article  Google Scholar 

  15. Ruggero, M. Responses to sound of the basilar membrane of the mammalian cochlea. Curr. Opin. Neurobiol. 2, 449–456 (1992).

    Article  CAS  Google Scholar 

  16. 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 

  17. Denk, W., Webb, W. W. & Hudspeth, A. J. Mechanical properties of sensory hair bundles are reflected in their Brownian motion measured with a laser differential interferometer. Proc. Natl Acad. Sci. USA 86, 5371– 5375 (1989).

    Article  CAS  Google Scholar 

  18. Hamill, O. P., Marty, A., Neher, E., Sakmann, B. & Sigworth, F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85–100 ( 1981).

    Article  CAS  Google Scholar 

  19. Howard, J. & Hudspeth, A. J. Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog's saccular hair cell. Proc. Natl Acad. Sci. USA 84, 3064–3068 (1987).

    Article  CAS  Google Scholar 

  20. Howard, J. & Ashmore, J. F. Stiffness of sensory hair bundles in the sacculus of the frog. Hear. Res. 23, 93–104 (1986).

    Article  CAS  Google Scholar 

  21. Atkins, P. W. in Physical Chemistry, (Oxford University Press, Oxford, 1978).

    Google Scholar 

  22. Howard, J., Roberts, W. M. & Hudspeth, A. J. Mechanoelectrical transduction by hair cells. Ann. Rev. Biophys. and Biophys. Chem. 17, 99– 124 (1988).

    Article  CAS  Google Scholar 

  23. Russell, I. J., Richardson, G. P. & Cody, A. R. Mechanosensitivity of mammalian auditory hair cells in vitro. Nature 321, 517– 519 (1986).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  25. Howard, J. & Hudspeth, A. J. Gating compliance associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron 1, 189– 199 (1988).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Assad, J. A., Hacohen, N. & Corey, D. P. Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc. Natl Acad. Sci. USA 86, 2918–2922 ( 1989).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Tim Cope and Ray Dingledine for critically reading the manuscript, Richard Jacobs for technical advice, and Mario Ruggero, Ille Gebeshuber and Peter Jung for discussions. This work was supported by the NIDCD and by a grant from the Emory/Georgia Tech. Consortium.

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  1. Dept. Physiology, Emory University School of Medicine , 1648 Pierce Dr., Atlanta, 30322, Georgia, USA

    Fernán Jaramillo

  2. School of Physics, Georgia Institute of Technology , Atlanta, 30332, Georgia, USA

    Kurt Wiesenfeld

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  1. Fernán Jaramillo
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  2. Kurt Wiesenfeld
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Correspondence to Fernán Jaramillo.

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Jaramillo, F., Wiesenfeld, K. Mechanoelectrical transduction assisted by Brownian motion: a role for noise in the auditory system. Nat Neurosci 1, 384–388 (1998). https://doi.org/10.1038/1597

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