Coherent, time-shifted patterns of microstructural plasticity during motor-skill learning
Michela Azzarito,
Tim M. Emmenegger,
Gabriel Ziegler,
Eveline Huber,
Patrick Grabher,
Martina F. Callaghan,
Alan Thompson,
Karl Friston,
Nikolaus Weiskopf,
Tim Killeen,
Patrick Freund
Affiliations
Michela Azzarito
Spinal Injury Center, University Hospital Balgrist, University of Zurich, Zurich, Switzerland; Contributed equally.
Tim M. Emmenegger
Spinal Injury Center, University Hospital Balgrist, University of Zurich, Zurich, Switzerland; Contributed equally.
Gabriel Ziegler
Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke-University Magdeburg, Magdeburg, Germany; German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany
Eveline Huber
Spinal Injury Center, University Hospital Balgrist, University of Zurich, Zurich, Switzerland
Patrick Grabher
Spinal Injury Center, University Hospital Balgrist, University of Zurich, Zurich, Switzerland
Martina F. Callaghan
Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom
Alan Thompson
Department of Neuroinflammation, UCL Institute of Neurology, University College London, London, United Kingdom
Karl Friston
Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom
Nikolaus Weiskopf
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany; Felix Bloch Institute for Solid State Physics, Faculty of Physics and Earth Sciences, Leipzig University, Leipzig, Germany
Tim Killeen
Spinal Injury Center, University Hospital Balgrist, University of Zurich, Zurich, Switzerland
Patrick Freund
Spinal Injury Center, University Hospital Balgrist, University of Zurich, Zurich, Switzerland; Wellcome Centre for Human Neuroimaging, UCL Queen Square Institute of Neurology, University College London, London, United Kingdom; Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany; Corresponding author at: Spinal Cord Injury Center, University Hospital Balgrist, Forchstrasse 340, 8008 Zurich, Switzerland.
Motor skill learning relies on neural plasticity in the motor and limbic systems. However, the spatial and temporal characteristics of these changes—and their microstructural underpinnings—remain unclear. Eighteen healthy males received 1 h of training in a computer-based motion game, 4 times a week, for 4 consecutive weeks, while 14 untrained participants underwent scanning only. Performance improvements were observed in all trained participants. Serial myelin- and iron-sensitive multiparametric mapping at 3T during this period of intensive motor skill acquisition revealed temporally and spatially distributed, performance-related microstructural changes in the grey and white matter across a corticospinal-cerebellar-hippocampal circuit. Analysis of the trajectory of these transient changes suggested time-shifted cascades of plasticity from the dominant sensorimotor system to the contralateral hippocampus. In the cranial corticospinal tracts, changes in myelin-sensitive metrics during training in the posterior limb of the internal capsule were of greater magnitude in those who trained their upper limbs vs. lower limb trainees. Motor skill learning is associated with waves of grey and white matter plasticity, across a broad sensorimotor network.
