Glycinergic axonal inhibition subserves acute spatial sensitivity to sudden increases in sound intensity

  1. Tom P Franken  Is a corresponding author
  2. Brian J Bondy
  3. David B Haimes
  4. Joshua Goldwyn
  5. Nace L Golding
  6. Philip H Smith
  7. Philip Joris  Is a corresponding author
  1. KU Leuven, Belgium
  2. UT Austin, United States
  3. Swarthmore College, United States
  4. University of Wisconsin-Madison, United States
  5. University of Leuven, Belgium

Abstract

Locomotion generates adventitious sounds which enable detection and localization of predators and prey. Such sounds contain brisk changes or transients in amplitude. We investigated the hypothesis that ill-understood temporal specializations in binaural circuits subserve lateralization of such sound transients, based on different time of arrival at the ears (interaural time differences, ITDs). We find that Lateral Superior Olive (LSO) neurons show exquisite ITD-sensitivity, reflecting extreme precision and reliability of excitatory and inhibitory postsynaptic potentials, in contrast to Medial Superior Olive neurons, traditionally viewed as the ultimate ITD-detectors. In vivo, inhibition blocks LSO excitation over an extremely short window, which, in vitro, required synaptically-evoked inhibition. Light and electron microscopy revealed inhibitory synapses on the axon initial segment as the structural basis of this observation. These results reveal a neural vetoing mechanism with extreme temporal and spatial precision and establish the LSO as the primary nucleus for binaural processing of sound transients.

Data availability

Source data files have been provided for all figures with electrophysiological recordings and for the computational model (Figures 1,2,3,4,7,8 and supplements). Custom MATLAB code for the computational model is provided as a source code file.

Article and author information

Author details

  1. Tom P Franken

    Department of Neuroscience, KU Leuven, Leuven, Belgium
    For correspondence
    tfranken@salk.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7160-5152
  2. Brian J Bondy

    Department of Neuroscience and Center for Learning and Memory, UT Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. David B Haimes

    Department of Neuroscience and Center for Learning and Memory, UT Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Joshua Goldwyn

    Department of Mathematics and Statistics, Swarthmore College, Swarthmore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5733-9089
  5. Nace L Golding

    Department of Neuroscience and Center for Learning and Memory, UT Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4072-310X
  6. Philip H Smith

    Department of Neuroscience, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Philip Joris

    University of Leuven, Leuven, Belgium
    For correspondence
    philip.joris@kuleuven.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9759-5375

Funding

Fonds Wetenschappelijk Onderzoek (Ph.D. fellowship)

  • Tom P Franken

Bijzonder Onderzoeksfonds KU Leuven (OT-14-118)

  • Philip Joris

Fonds Wetenschappelijk Onderzoek (G.0961.11)

  • Philip Joris

Fonds Wetenschappelijk Onderzoek (G.0A11.13)

  • Philip Joris

Fonds Wetenschappelijk Onderzoek (G.091214N)

  • Philip Joris

National Institute on Deafness and Other Communication Disorders (DC006212)

  • Philip H Smith
  • Philip Joris

National Institute on Deafness and Other Communication Disorders (DC011403)

  • Nace L Golding
  • Philip Joris

National Institute on Deafness and Other Communication Disorders (DC006788)

  • Nace L Golding

National Institute on Deafness and Other Communication Disorders (1F31DC017377-01)

  • David B Haimes

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

Reviewing Editor

  1. Catherine Emily Carr, University of Maryland, United States

Ethics

Animal experimentation: This study was performed in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All in vivo procedures were approved by the KU Leuven Ethics Committee for Animal Experiments (protocol numbers P155/2008, P123/2010, P167/2012, P123/2013, P005/2014). All in vitro recording and immunohistochemistry experiments were approved by the University of Texas at Austin Animal Care and Use Committee in compliance with the recommendations of the United States National Institutes of Health.

Version history

  1. Received: August 17, 2020
  2. Accepted: June 12, 2021
  3. Accepted Manuscript published: June 14, 2021 (version 1)
  4. Version of Record published: June 28, 2021 (version 2)

Copyright

© 2021, Franken 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. Tom P Franken
  2. Brian J Bondy
  3. David B Haimes
  4. Joshua Goldwyn
  5. Nace L Golding
  6. Philip H Smith
  7. Philip Joris
(2021)
Glycinergic axonal inhibition subserves acute spatial sensitivity to sudden increases in sound intensity
eLife 10:e62183.
https://doi.org/10.7554/eLife.62183

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https://doi.org/10.7554/eLife.62183

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