Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity

  1. Maria Cristina Perez-Flores
  2. Eric Verschooten
  3. Jeong Han Lee
  4. Hyo Jeong Kim
  5. Philip X Joris
  6. Ebenezer N Yamoah  Is a corresponding author
  1. University of Nevada Reno, United States
  2. University of Leuven, Belgium

Abstract

Mechanosensation - by which mechanical stimuli are converted into a neuronal signal - is the basis for the sensory systems of hearing, balance, and touch. Mechanosensation is unmatched in speed and its diverse range of sensitivities, reaching its highest temporal limits with the sense of hearing; however, hair cells (HCs) and the auditory nerve (AN) serve as obligatory bottlenecks for sounds to engage the brain. Like other sensory neurons, auditory neurons use the canonical pathway for neurotransmission and millisecond-duration action potentials (APs). How the auditory system utilizes the relatively slow transmission mechanisms to achieve ultrafast speed, and high audio-frequency hearing remains an enigma. Here, we address this paradox and report that the mouse, and chinchilla, AN are mechanically sensitive, and minute mechanical displacement profoundly affects its response properties. Sound-mimicking sinusoidal mechanical and electrical current stimuli affect phase-locked responses. In a phase-dependent manner, the two stimuli can also evoke suppressive responses. We propose that mechanical sensitivity interacts with synaptic responses to shape responses in the AN, including frequency tuning and temporal phase-locking. Combining neurotransmission and mechanical sensation to control spike patterns gives the mammalian AN a secondary receptor role, an emerging theme in primary neuronal functions.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 1-4

Article and author information

Author details

  1. Maria Cristina Perez-Flores

    University of Nevada Reno, Reno, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Eric Verschooten

    Laboratory of Auditory Neurophysiology, University of Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  3. Jeong Han Lee

    University of Nevada Reno, Reno, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Hyo Jeong Kim

    University of Nevada Reno, Reno, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Philip X Joris

    Laboratory of Auditory Neurophysiology, University of Leuven, Leuven, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  6. Ebenezer N Yamoah

    University of Nevada Reno, Reno, United States
    For correspondence
    enyamoah@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9797-085X

Funding

National Institute of Health (DC016099,DC015252,DC015135,AG060504,AG051443)

  • Ebenezer N Yamoah

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

Reviewing Editor

  1. Tobias Reichenbach, Friedrich-Alexander-University (FAU) Erlangen-Nürnberg, Germany

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#08-133) of the University of Arizona. The protocol was approved by the Committee on the Ethics of Animal Experiments of the University of Minnesota (Permit Number: 27-2956). All surgery was performed under sodium pentobarbital anesthesia, and every effort was made to minimize suffering (Yamoah, UNR protocol).

Version history

  1. Preprint posted: May 18, 2021 (view preprint)
  2. Received: October 22, 2021
  3. Accepted: March 9, 2022
  4. Accepted Manuscript published: March 10, 2022 (version 1)
  5. Version of Record published: March 23, 2022 (version 2)

Copyright

© 2022, Perez-Flores 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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  1. Maria Cristina Perez-Flores
  2. Eric Verschooten
  3. Jeong Han Lee
  4. Hyo Jeong Kim
  5. Philip X Joris
  6. Ebenezer N Yamoah
(2022)
Intrinsic mechanical sensitivity of mammalian auditory neurons as a contributor to sound-driven neural activity
eLife 11:e74948.
https://doi.org/10.7554/eLife.74948

Share this article

https://doi.org/10.7554/eLife.74948

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