Abstract
The discrepancies between measured frequency responses of the basilar membrane in the inner ear and the frequency tuning found in psychophysical experiments led to Békésy's idea of lateral inhibition in the auditory nervous system1. We now know that basilar membrane tuning can account for neural tuning2, and that sharpening of the passive travelling wave depends on the mechanical activity of outer hair cells (OHCs)3, but the mechanism by which OHCs enhance tuning remains unclear. OHCs generate voltage-dependent length changes at acoustic rates4,5,6,7,8, which deform the cochlear partition9,10,11. Here we use an electrical correlate of OHC mechanical activity, the motility-related gating current, to investigate mechano-electrical interactions among adjacent OHCs. We show that the motility caused by voltage stimulation of one cell in a group evokes gating currents in adjacent OHCs. The resulting polarization in adjacent cells is opposite to that within the stimulated cell, which may be indicative of lateral inhibition. Also such interactions promote distortion and suppression in the electrical and, consequently, the mechanical activity of OHCs. Lateral interactions may provide a basis for enhanced frequency selectivity in the basilar membrane of mammals.
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References
von Békésy, G. Experiments in Hearing (McGraw-Hill, New York, (1960 ).
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).
Dallos, P. The active cochlea. J. Neurosci. 12, 4575 –4585 (1992).
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).
Santos-Sacchi, J. & Dilger, J. P. Whole cell currents and mechanical responses of isolated outer hair cells. Hear. Res. 35, 143–150 ( 1988).
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).
Dallos, P. & Evans, B. N. High frequency motility of outer hair cells and the cochlear amplifier. Science 267, 2006–2009 (1995).
Gale, J. E. & Ashmore, J. F. An intrinsic frequency limit to the cochlea amplifier. Nature 389, 63 –66 (1997).
Xue, S., Mountain, D. C. & Hubbard, A. E. Electrically evoked basilar membrane motion. J. Acoust. Soc. Am. 97, 3030–3041 (1995).
Nuttall, A. L. & Ren, T. Electromotile hearing: evidence from basilar membrane motion and otoacoustic emissions. Hear. Res. 92, 170–177 ( 1995).
Mammano, F. & Ashmore, J. F. Reverse transduction measured in the isolated cochlea by laser Michelson interferometry. Nature 365, 838–841 ( 1993).
Ashmore, J. F. Forward and reverse transduction in the mammalian cochlea. Neurosci. Res. (suppl.) 12, 39–50 (1990).
Santos-Sacchi, J. Reversible inhibition of voltage dependent outer hair cell motility and capacitance. J.Neurosci. 11, 3096–3110 (1991).
Iwasa, K. H. Effect of stress on the membrane capacitance of the auditory outer hair cell. Biophys. J. 65, 492–498 (1993).
Gale, J. E. & Ashmore, J. F. Charge displacement induced by rapid stretch in the basolateral membrane of the guinea-pig outer hair cell. Proc. R. Soc. Lond. B 255, 243– 249 (1994).
Kakehata, S. & Santos-Sacchi, J. Membrane tension directly shifts voltage dependence of outer hair cell motility and associated gating charge. Biophys. J. 68, 2190– 2197 (1995).
Vater, M., Lenoir, M. & Pujol, R. Ultrastructure of the horseshoe bat's organ of Corti. II. Transmission electron microscopy. J. Comp. Neurol. 318, 380–391 (1992).
Huang, G.-J. & Santos-Sacchi, J. Mapping the distribution of the outer hair cell motility voltage sensor by electrical amputation. Biophys. J. 65, 2228–2236 (1993).
Huang, G.-J. & Santos-Sacchi, J. Motility voltage sensor of the outer hair cell resides within the lateral plasma membrane. Proc. Natl Acad. Sci. USA 91, 12268– 12272 (1994).
Tunstall, M. J., Gale, J. E. & Ashmore, J. F. Action of salicylate on membrane capacitance of outer hair cells from the guinea-pig cochlea. J. Physiol. (Lond.) 485, 739–752 (1995).
Kakehata, S. & Santos-Sacchi, J. Effects of lanthanides and salicylate on outer hair cell motility and associated gating charge. J. Acoust. Soc. Am. 41, 676–689 (1967).
Goldstein, J. L. Auditory nonlinearity. J. Acoust. Soc. Am. 41, 676–689 (1967).
Goldstein, J. L. & Kiang, N. Y. S. Neural correlates of the aural combination tone 2f1-f2. Proc. IEEE 56 , 981–992 (1968).
Dallos, P. & Harris, D. in Psychophysics and Physiology of Hearing (eds Evans, E. F. & Wilson, J. P.) 147 (Academic, London, (1977).
Dallos, P., Harris, D. M., Relkin, E. & Cheatham, M. A. in Psychophysical Physiological and Behavioural Studies in Hearing (eds van den Brink, G. & Bilsen, F. A.) 242–249 (Delft Univ. Press, Holland, (1980).
Jaramillo, F., Markin, V. S. & Hudspeth, A. J. Auditory illusions and the single hair cell. Nature 364, 527–529 ( 1993).
Takahashi, S. & Santos-Sacchi, J. Distortion component analysis of outer hair cell motility-related gating charge. J. Membr. Biol. (in the press).
Santos-Sacchi, J. Harmonics of outer hair cell motility. Biophys. J. 65, 2217–2227 (1993).
Santos-Sacchi, J., Kakehata, S. & Takahashi, S. The outer hair cell membrane potential directly affects the voltage dependence of motility-related gating charge. J. Physiol. (Lond.) 510, 225–235 ( 1998).
Bezanilla, F. & Armstrong, C. M. Inactivation of the sodium channel. I. Sodium current experiments. J. Gen. Physiol. 70, 549–566 (1977).
Acknowledgements
We thank M. Mazzucco for technical help. This work was supported by a grant from NINCDS to J.S.S.
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Zhao, HB., Santos-Sacchi, J. Auditory collusion and a coupled couple of outer hair cells. Nature 399, 359–362 (1999). https://doi.org/10.1038/20686
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DOI: https://doi.org/10.1038/20686
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