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Coherent motion of stereocilia assures the concerted gating of hair-cell transduction channels

Nature Neuroscience volume 10, pages 87–92 (2007)Cite this article

Abstract

The hair cell's mechanoreceptive organelle, the hair bundle, is highly sensitive because its transduction channels open over a very narrow range of displacements. The synchronous gating of transduction channels also underlies the active hair-bundle motility that amplifies and tunes responsiveness. The extent to which the gating of independent transduction channels is coordinated depends on how tightly individual stereocilia are constrained to move as a unit. Using dual-beam interferometry in the bullfrog's sacculus, we found that thermal movements of stereocilia located as far apart as a hair bundle's opposite edges showed high coherence and negligible phase lag. Because the mechanical degrees of freedom of stereocilia are strongly constrained, a force applied anywhere in the hair bundle deflects the structure as a unit. This feature assures the concerted gating of transduction channels that maximizes the sensitivity of mechanoelectrical transduction and enhances the hair bundle's capacity to amplify its inputs.

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Figure 1: The hair bundle and its possible modes of motion.
Figure 2: Experimental preparation and control measurements.
Figure 3: Coherency of stereociliary motion for quiescent hair bundles.
Figure 4: Coherency of stereociliary motion for oscillating hair bundles.
Figure 5: Effect of severing tip links on hair-bundle motion.
Figure 6: Modeling of hair-bundle movements.

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Acknowledgements

The authors thank A.J. Hinterwirth for assistance in constructing the interferometer, B. Fabella for programming the experimental software and O. Ahmad, M.O. Magnasco, K. Purpura and J. Victor for useful discussions. The members of our research group provided helpful comments on the manuscript. The research reported in this paper was funded by the US National Institutes of Health. T.R. was supported by funding from the F.M. Kirby Foundation and from the US National Institutes of Health. A.S.K. was supported by Howard Hughes Medical Institute, of which A.J.H. is an Investigator.

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Author notes

  1. Thomas Risler

    Present address: Laboratoire Physicochimie Curie UMR 168, Institut Curie section de Recherche, 26 rue d'Ulm, F-75248, Paris Cedex, 05, France

  2. Andrei S Kozlov and Thomas Risler: These authors contributed equally to this work.

Authors and Affiliations

  1. Howard Hughes Medical Institute and Laboratory of Sensory Neuroscience, The Rockefeller University, 1230 York Avenue, New York, 10021, New York, USA

    Andrei S Kozlov, Thomas Risler & A J Hudspeth

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A.J.H. conceived the experiments, A.S.K. performed them and T.R. conducted the data analysis. A.S.K., T.R. and A.J.H. wrote the paper.

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Correspondence to A J Hudspeth.

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The authors declare no competing financial interests.

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Kozlov, A., Risler, T. & Hudspeth, A. Coherent motion of stereocilia assures the concerted gating of hair-cell transduction channels. Nat Neurosci 10, 87–92 (2007). https://doi.org/10.1038/nn1818

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