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

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 command...

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Main Authors: Jean Laurens, Dora E Angelaki
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/28074
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spelling doaj-4ba63fb0db804d3b8499d07cf4ef02452021-05-05T13:52:37ZengeLife Sciences Publications LtdeLife2050-084X2017-10-01610.7554/eLife.28074A unified internal model theory to resolve the paradox of active versus passive self-motion sensationJean Laurens0https://orcid.org/0000-0002-9101-2802Dora E Angelaki1https://orcid.org/0000-0002-9650-8962Department of Neuroscience, Baylor College of Medicine, Houston, United StatesDepartment of Neuroscience, Baylor College of Medicine, Houston, United StatesBrainstem 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.https://elifesciences.org/articles/28074bayesianvestibularefference copyvestibular nucleuscerebelluminternal model
collection DOAJ
language English
format Article
sources DOAJ
author Jean Laurens
Dora E Angelaki
spellingShingle Jean Laurens
Dora E Angelaki
A unified internal model theory to resolve the paradox of active versus passive self-motion sensation
eLife
bayesian
vestibular
efference copy
vestibular nucleus
cerebellum
internal model
author_facet Jean Laurens
Dora E Angelaki
author_sort Jean Laurens
title A unified internal model theory to resolve the paradox of active versus passive self-motion sensation
title_short A unified internal model theory to resolve the paradox of active versus passive self-motion sensation
title_full A unified internal model theory to resolve the paradox of active versus passive self-motion sensation
title_fullStr A unified internal model theory to resolve the paradox of active versus passive self-motion sensation
title_full_unstemmed A unified internal model theory to resolve the paradox of active versus passive self-motion sensation
title_sort unified internal model theory to resolve the paradox of active versus passive self-motion sensation
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-10-01
description 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.
topic bayesian
vestibular
efference copy
vestibular nucleus
cerebellum
internal model
url https://elifesciences.org/articles/28074
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