Brain-spinal cord interaction in long-term motor sequence learning in human: an fMRI Study

Ali Khatibi, Shahabeddin Vahdat, Ovidiu Lungu, Jürgen Finsterbusch, Christian Büchel, Julien Cohen-Adad, Veronique Marchand-Pauvert, Julien Doyon

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Abstract

The spinal cord is important for sensory guidance and execution of skilled movements. Yet its role in human motor learning is not well understood. Despite evidence revealing an active involvement of spinal circuits in the early phase of motor learning, whether long-term learning engages similar changes in spinal cord activation and functional connectivity remains unknown. Here, we investigated spinal–cerebral functional plasticity associated with learning of a specific sequence of visually-guided joystick movements (sequence task) over six days of training. On the first and last training days, we acquired high-resolution functional images of the brain and cervical cord simultaneously, while participants practiced the sequence or a random task while electromyography was recorded from wrist muscles. After six days of training, the subjects’ motor performance improved in the sequence compared to the control condition. These behavioral changes were associated with decreased co-contractions and increased reciprocal activations between antagonist wrist muscles. Importantly, early learning was characterized by activation in the C8 level, whereas a more rostral activation in the C6-C7 was found during the later learning phase. Motor sequence learning was also supported by increased spinal cord functional connectivity with distinct brain networks, including the motor cortex, superior parietal lobule, and the cerebellum at the early stage, and the angular gyrus and cerebellum at a later stage of learning. Our results suggest that the early vs. late shift in spinal activation from caudal to rostral cervical segments synchronized with distinct brain networks, including parietal and cerebellar regions, is related to progressive changes reflecting the increasing fine control of wrist muscles during motor sequence learning.
Original languageEnglish
Article number119111
JournalNeuroImage
Volume253
Early online date21 Mar 2022
DOIs
Publication statusPublished - Jun 2022

Bibliographical note

Funding Information:
We would like to thank Mr Benoit Beranger for his help in the preprocessing of EMG data acquired inside the scanner. We also would like to thank Mr Arnaud Boré for his help at different stages of this work and Mr Chadi Sayour for his contribution at data collection stage of the project.

Publisher Copyright:
© 2022 The Author(s)

Keywords

  • Brain
  • Motor learning
  • Networks
  • Spinal cord
  • fMRI

ASJC Scopus subject areas

  • Neurology
  • Cognitive Neuroscience

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