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Coherent waves of myelin plasticity during motor-skill learning

Michela Azzarito, Gabriel Ziegler, Eveline Huber, Patrick Grabher, Martina F. Callaghan, Alan Thompson, Karl Friston, Nikolaus Weiskopf, Tim Killeen, Patrick Freund
doi: https://doi.org/10.1101/2021.04.13.439402
Michela Azzarito
1Spinal Cord Injury Center Balgrist, University Hospital Zurich, University of Zurich, Zurich, Switzerland
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Gabriel Ziegler
2Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke-University Magdeburg, Magdeburg, Germany
3German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
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Eveline Huber
1Spinal Cord Injury Center Balgrist, University Hospital Zurich, University of Zurich, Zurich, Switzerland
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Patrick Grabher
1Spinal Cord Injury Center Balgrist, University Hospital Zurich, University of Zurich, Zurich, Switzerland
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Martina F. Callaghan
4Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, UK
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Alan Thompson
5Department of Brain Repair and Rehabilitation, UCL Institute of Neurology, University College London, London, UK
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Karl Friston
4Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, UK
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Nikolaus Weiskopf
6Departments of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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Tim Killeen
1Spinal Cord Injury Center Balgrist, University Hospital Zurich, University of Zurich, Zurich, Switzerland
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Patrick Freund
1Spinal Cord Injury Center Balgrist, University Hospital Zurich, University of Zurich, Zurich, Switzerland
4Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, UK
5Department of Brain Repair and Rehabilitation, UCL Institute of Neurology, University College London, London, UK
6Departments of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
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  • For correspondence: patrick.freund@balgrist.ch
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Abstract

Motor skill learning relies on neural plasticity in the motor and limbic systems. However, the spatial and temporal dependencies of these changes—and their microstructural underpinnings—remain unclear. Eighteen healthy males received training in a computer-controlled motion game 4 times a week, for 4 weeks. Performance improvements were observed in all trained participants. Serial myelin-sensitive multiparametric mapping at 3T during this period of intensive motor skill acquisition revealed temporally and spatially distributed, performance-related myelin-sensitive microstructural changes in the grey and white matter across the corticospinal system and hippocampus. Interestingly, analysis of the trajectory of these transient changes revealed a time-shifted choreography across white and grey matter of the corticospinal system as well as with changes in the hippocampus. Crucially, in the cranial corticospinal tracts, myelin-sensitive changes during training in the posterior part of the limb of the internal capsule were of greater magnitude in lower-limb trainees compared to upper limb trainees. Motor skill learning is depended on coherent waves of plasticity within a corticospinal-hippocampal loop.

Competing Interest Statement

The authors have declared no competing interest.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted April 14, 2021.
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Coherent waves of myelin plasticity during motor-skill learning
Michela Azzarito, Gabriel Ziegler, Eveline Huber, Patrick Grabher, Martina F. Callaghan, Alan Thompson, Karl Friston, Nikolaus Weiskopf, Tim Killeen, Patrick Freund
bioRxiv 2021.04.13.439402; doi: https://doi.org/10.1101/2021.04.13.439402
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Coherent waves of myelin plasticity during motor-skill learning
Michela Azzarito, Gabriel Ziegler, Eveline Huber, Patrick Grabher, Martina F. Callaghan, Alan Thompson, Karl Friston, Nikolaus Weiskopf, Tim Killeen, Patrick Freund
bioRxiv 2021.04.13.439402; doi: https://doi.org/10.1101/2021.04.13.439402

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