1. Neuroscience
  2. Physics of Living Systems
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Stiffness and tension gradients of the hair cell's tip-link complex in the mammalian cochlea

  1. Mélanie Tobin
  2. Atitheb Chaiyasitdhi
  3. Vincent Michel
  4. Nicolas Antoine Michalski
  5. Pascal Martin  Is a corresponding author
  1. PSL Research University, France
  2. Sorbonne Université, France
Research Article
  • Cited 7
  • Views 1,518
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Cite this article as: eLife 2019;8:e43473 doi: 10.7554/eLife.43473

Abstract

Sound analysis by the cochlea relies on frequency tuning of mechanosensory hair cells along a tonotopic axis. To clarify the underlying biophysical mechanism, we have investigated the micromechanical properties of the hair cell's mechanoreceptive hair bundle within the apical half of the rat cochlea. We studied both inner and outer hair cells, which send nervous signals to the brain and amplify cochlear vibrations, respectively. We find that tonotopy is associated with gradients of stiffness and resting mechanical tension, with steeper gradients for outer hair cells, emphasizing the division of labor between the two hair-cell types. We demonstrate that tension in the tip links that convey force to the mechano-electrical transduction channels increases at reduced Ca2+. Finally, we reveal gradients in stiffness and tension at the level of a single tip link. We conclude that mechanical gradients of the tip-link complex may help specify the characteristic frequency of the hair cell.

Article and author information

Author details

  1. Mélanie Tobin

    Laboratoire Physico-Chimie Curie, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Atitheb Chaiyasitdhi

    Laboratoire Physico-Chimie Curie, PSL Research University, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Vincent Michel

    Sorbonne Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicolas Antoine Michalski

    Sorbonne Université, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1287-2709
  5. Pascal Martin

    Laboratoire Physico-Chimie Curie, PSL Research University, Paris, France
    For correspondence
    pascal.martin@curie.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6860-4677

Funding

French National Agency for Research (ANR-11-BSV5-011)

  • Pascal Martin

Labex Celltisphybio part of the Idex PSL (ANR-10-LABX-0038)

  • Pascal Martin

French National Agency for Research (ANR-16-CE13-0015)

  • Pascal Martin

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experimental procedures were approved by the Ethics committee on animal experimentation of the Institut Curie; they complied with the European and French-National Regulation for the Protection of Vertebrate Animals used for Experimental and other Scientific Purposes (Directive 2010/63; French Decree 2013-118).

Reviewing Editor

  1. Doris K Wu, National Institutes of Health, United States

Publication history

  1. Received: November 7, 2018
  2. Accepted: March 27, 2019
  3. Accepted Manuscript published: April 1, 2019 (version 1)
  4. Version of Record published: April 15, 2019 (version 2)

Copyright

© 2019, Tobin et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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Further reading

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    Adhesion-type GPCRs (aGPCRs) participate in a vast range of physiological processes. Their frequent association with mechanosensitive functions suggests that processing of mechanical stimuli may be a common feature of this receptor family. Previously, we reported that the Drosophila aGPCR CIRL sensitizes sensory responses to gentle touch and sound by amplifying signal transduction in low-threshold mechanoreceptors (Scholz et al., 2017). Here, we show that Cirl is also expressed in high-threshold mechanical nociceptors where it adjusts nocifensive behaviour under physiological and pathological conditions. Optogenetic in vivo experiments indicate that CIRL lowers cAMP levels in both mechanosensory submodalities. However, contrasting its role in touch-sensitive neurons, CIRL dampens the response of nociceptors to mechanical stimulation. Consistent with this finding, rat nociceptors display decreased Cirl1 expression during allodynia. Thus, cAMP-downregulation by CIRL exerts opposing effects on low-threshold mechanosensors and high-threshold nociceptors. This intriguing bipolar action facilitates the separation of mechanosensory signals carrying different physiological information.