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.

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).

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.

Metrics

  • 1,332
    views
  • 233
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Neuroscience
    Lenia Amaral, Xiaosha Wang ... Ella Striem-Amit
    Research Article

    Research on brain plasticity, particularly in the context of deafness, consistently emphasizes the reorganization of the auditory cortex. But to what extent do all individuals with deafness show the same level of reorganization? To address this question, we examined the individual differences in functional connectivity (FC) from the deprived auditory cortex. Our findings demonstrate remarkable differentiation between individuals deriving from the absence of shared auditory experiences, resulting in heightened FC variability among deaf individuals, compared to more consistent FC in the hearing group. Notably, connectivity to language regions becomes more diverse across individuals with deafness. This does not stem from delayed language acquisition; it is found in deaf native signers, who are exposed to natural language since birth. However, comparing FC diversity between deaf native signers and deaf delayed signers, who were deprived of language in early development, we show that language experience also impacts individual differences, although to a more moderate extent. Overall, our research points out the intricate interplay between brain plasticity and individual differences, shedding light on the diverse ways reorganization manifests among individuals. It joins findings of increased connectivity diversity in blindness and highlights the importance of considering individual differences in personalized rehabilitation for sensory loss.

    1. Computational and Systems Biology
    2. Neuroscience
    Gabriel Loewinger, Erjia Cui ... Francisco Pereira
    Tools and Resources

    Fiber photometry has become a popular technique to measure neural activity in vivo, but common analysis strategies can reduce the detection of effects because they condense within-trial signals into summary measures, and discard trial-level information by averaging across-trials. We propose a novel photometry statistical framework based on functional linear mixed modeling, which enables hypothesis testing of variable effects at every trial time-point, and uses trial-level signals without averaging. This makes it possible to compare the timing and magnitude of signals across conditions while accounting for between-animal differences. Our framework produces a series of plots that illustrate covariate effect estimates and statistical significance at each trial time-point. By exploiting signal autocorrelation, our methodology yields joint 95% confidence intervals that account for inspecting effects across the entire trial and improve the detection of event-related signal changes over common multiple comparisons correction strategies. We reanalyze data from a recent study proposing a theory for the role of mesolimbic dopamine in reward learning, and show the capability of our framework to reveal significant effects obscured by standard analysis approaches. For example, our method identifies two dopamine components with distinct temporal dynamics in response to reward delivery. In simulation experiments, our methodology yields improved statistical power over common analysis approaches. Finally, we provide an open-source package and analysis guide for applying our framework.