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Neural variability determines coding strategies for natural self-motion in macaque monkeys

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Cite this article as: eLife 2020;9:e57484 doi: 10.7554/eLife.57484

Abstract

We have previously reported that central neurons mediating vestibulo-spinal reflexes and self-motion perception optimally encode natural self-motion (Mitchell et al., 2018). Importantly however, the vestibular nuclei also comprise other neuronal classes that mediate essential functions such as the vestibulo-ocular reflex (VOR) and its adaptation. Here we show that heterogeneities in resting discharge variability mediate a trade-off between faithful encoding and optimal coding via temporal whitening. Specifically, neurons displaying lower variability did not whiten naturalistic self-motion but instead faithfully represented the stimulus' detailed time course, while neurons displaying higher variability displayed temporal whitening. Using a well-established model of VOR pathways, we demonstrate that faithful stimulus encoding is necessary to generate the compensatory eye movements found experimentally during naturalistic self-motion. Our findings suggest a novel functional role for variability towards establishing different coding strategies: 1) faithful stimulus encoding for generating the VOR; 2) optimized coding via temporal whitening for other vestibular functions.

Article and author information

Author details

  1. Isabelle Mackrous

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

    Department of Physiology, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Kathleen E Cullen

    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:" 0000-0002-9348-0933
  4. Maurice J Chacron

    Department of Physiology, McGill University, Montreal, Canada
    For correspondence
    maurice.chacron@mcgill.ca
    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

Funding

Canadian Institutes of Health Research (162285)

  • Jérome Carriot
  • Kathleen E Cullen
  • Maurice J Chacron

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 (#4096) and complied with the guidelines of the Canadian Council on Animal Care.

Reviewing Editor

  1. Fred Rieke, University of Washington, United States

Publication history

  1. Received: April 2, 2020
  2. Accepted: September 10, 2020
  3. Accepted Manuscript published: September 11, 2020 (version 1)

Copyright

© 2020, Mackrous 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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