Coding strategies in the otolith system differ for translational head motion vs static orientation relative to gravity

Abstract

The detection of gravito-inertial forces by the otolith system is essential for our sense of balance and accurate perception. To date, however, how this system encodes self-motion stimuli experienced during everyday activities remains unknown. Here we directly addressed this fundamental question by recording from single otolith afferents in monkeys during naturalistic translational self-motion and changes in static head orientation. Otolith afferents with higher intrinsic variability transmitted overall more information about translational self-motion than their regular counterparts, due to stronger nonlinearities that enabled precise spike timing including phase locking. In contrast, more regular afferents better discriminated between different static head orientations relative to gravity. Using computational methods, we further demonstrated that coupled increases in intrinsic variability and sensitivity accounted for observed functional differences between afferent classes. Together, our results indicate that irregular and regular otolith afferents may use different strategies to encode naturalistic self-motion and static head orientation relative to gravity.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data and Matlab codes have been deposited on Figshare under the URL: https://doi.org/10.6084/m9.figshare.8251613.v1

The following data sets were generated

Article and author information

Author details

  1. Mohsen Jamali

    Department of Physiology, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Jerome Carriot

    Department of Physiology, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Maurice J Chacron

    Department of Physiology, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3032-452X
  4. Kathleen E Cullen

    Department of Physiology, McGill University, Montreal, Canada
    For correspondence
    kathleen.cullen@jhu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9348-0933

Funding

Canadian Institutes of Health Research

  • Kathleen E Cullen

Canadian Institutes of Health Research

  • Maurice J Chacron

Canada Research Chairs

  • Maurice J Chacron

National Institutes of Health (DC2390)

  • Kathleen E Cullen

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 protocols were approved by the McGill University Animal Care Committee (#2001-4096) and were in compliance with the guidelines of the Canadian Council on Animal Care. Two male macaque monkeys (Macaca fascicularis) were prepared for chronic extracellular recording under aseptic conditions. The surgical preparation was similar to that previously described (Dale & Cullen, 2013). Animals (aged 6 and 8 years old) were housed in pairs on a 12 hour light/dark cycle

Reviewing Editor

  1. Joshua I Gold, University of Pennsylvania, United States

Publication history

  1. Received: January 28, 2019
  2. Accepted: June 13, 2019
  3. Accepted Manuscript published: June 14, 2019 (version 1)
  4. Version of Record published: June 24, 2019 (version 2)

Copyright

© 2019, Jamali 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. Mohsen Jamali
  2. Jerome Carriot
  3. Maurice J Chacron
  4. Kathleen E Cullen
(2019)
Coding strategies in the otolith system differ for translational head motion vs static orientation relative to gravity
eLife 8:e45573.
https://doi.org/10.7554/eLife.45573
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