Neuronal variability and tuning are balanced to optimize naturalistic self-motion coding in primate vestibular pathways

Abstract

It is commonly assumed that the brain's neural coding strategies are adapted to the statistics of natural stimuli. Specifically, to maximize information transmission, a sensory neuron's tuning function should effectively oppose the decaying stimulus spectral power, such that the neural response is temporally decorrelated (i.e., 'whitened'). However, theory predicts that the structure of neuronal variability also plays an essential role in determining how coding is optimized. Here, we provide experimental evidence supporting this view by recording from neurons in early vestibular pathways during naturalistic self-motion. We found that central vestibular neurons displayed temporally whitened responses that could not be explained by their tuning alone. Rather, computational modeling and analysis revealed that neuronal variability and tuning were matched to effectively complement natural stimulus statistics, thereby achieving temporal decorrelation and optimizing information transmission. Taken together, our findings reveal a novel strategy by which neural variability contributes to optimized processing of naturalistic stimuli.

Data availability

All data have been deposited on Figshare under the URL https://doi.org/10.6084/m9.figshare.7423724.v1.

The following data sets were generated

Article and author information

Author details

  1. Diana E Mitchell

    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:" 0000-0003-0733-484X
  2. Annie Kwan

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

    Department of Physiology, McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. 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
  5. 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

  • Maurice J Chacron
  • Kathleen E Cullen

Canada Research Chairs

  • Maurice J Chacron

National Institutes of Health

  • 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. Three male macaque monkeys (2 Macaca mulatta and 1 Macaca fascicularis) were prepared for chronic extracellular recording using aseptic surgical techniques as previously described (Massot et al., 2011). Animals (aged 7, 8, and 8 years old) were housed in pairs on a 12 hour light/dark cycle.

Reviewing Editor

  1. Fred Rieke, University of Washington, United States

Publication history

  1. Received: October 22, 2018
  2. Accepted: December 17, 2018
  3. Accepted Manuscript published: December 18, 2018 (version 1)
  4. Version of Record published: December 31, 2018 (version 2)

Copyright

© 2018, Mitchell 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. Diana E Mitchell
  2. Annie Kwan
  3. Jerome Carriot
  4. Maurice J Chacron
  5. Kathleen E Cullen
(2018)
Neuronal variability and tuning are balanced to optimize naturalistic self-motion coding in primate vestibular pathways
eLife 7:e43019.
https://doi.org/10.7554/eLife.43019
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