A unified internal model theory to resolve the paradox of active versus passive self-motion sensation

  1. Jean Laurens  Is a corresponding author
  2. Dora E Angelaki
  1. Baylor College of Medicine, United States

Abstract

Brainstem and cerebellar neurons implement an internal model to accurately estimate self-motion during externally-generated ('passive') movements. However, these neurons show reduced responses during self-generated ('active') movements, indicating that predicted sensory consequences of motor commands cancel sensory signals. Remarkably, the computational processes underlying sensory prediction during active motion and their relationship to internal model computations during passive movements remain unknown. We construct a Kalman filter that incorporates motor commands into a previously-established model of optimal passive self-motion estimation. The simulated sensory error and feedback signals match experimentally measured neuronal responses during active and passive head and trunk rotations and translations. We conclude that a single sensory internal model can combine motor commands with vestibular and proprioceptive signals optimally. Thus, although neurons carrying sensory prediction error or feedback signals show attenuated modulation, the sensory cues and internal model are both engaged and critically important for accurate self-motion estimation during active head movements.

Article and author information

Author details

  1. Jean Laurens

    Department of Neuroscience, Baylor College of Medicine, Houston, United States
    For correspondence
    jean.laurens@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9101-2802
  2. Dora E Angelaki

    Department of Neuroscience, Baylor College of Medicine, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9650-8962

Funding

National Institute on Deafness and Other Communication Disorders (NIH R01DC004260)

  • Dora E Angelaki

National Institute on Deafness and Other Communication Disorders (NIH R01DC004260)

  • Jean Laurens

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

Reviewing Editor

  1. Stefan Glasauer

Publication history

  1. Received: April 25, 2017
  2. Accepted: October 11, 2017
  3. Accepted Manuscript published: October 18, 2017 (version 1)
  4. Version of Record published: November 14, 2017 (version 2)

Copyright

© 2017, Laurens & Angelaki

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. Jean Laurens
  2. Dora E Angelaki
(2017)
A unified internal model theory to resolve the paradox of active versus passive self-motion sensation
eLife 6:e28074.
https://doi.org/10.7554/eLife.28074

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