Brain-spinal cord interaction in long-term motor sequence learning in human: An fMRI study
Ali Khatibi,
Shahabeddin Vahdat,
Ovidiu Lungu,
Jurgen Finsterbusch,
Christian Büchel,
Julien Cohen-Adad,
Veronique Marchand-Pauvert,
Julien Doyon
Affiliations
Ali Khatibi
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada; Centre de recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada; Centre of Precision Rehabilitation for Spinal Pain (CPR Spine), University of Birmingham, UK; Centre for Human Brain Health, University of Birmingham, UK; Corresponding author.
Shahabeddin Vahdat
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada; Centre de recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada; Department of Applied Physiology and Kinesiology, University of Florida, Gainesville, FL, USA
Ovidiu Lungu
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada; Centre de recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada; Department of psychiatry and addictology, University of Montreal, Montreal, QC, Canada
Jurgen Finsterbusch
Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Germany
Christian Büchel
Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, Germany
Julien Cohen-Adad
NeuroPoly Lab, Institute of Biomedical Engineering, Polytechnique Montreal, Montreal, QC, Canada; Functional Neuroimaging Unit, CRIUGM, University of Montreal, Montreal, QC, Canada; Mila Quebec AI Institute, Montreal, QC, Canada
McConnell Brain Imaging Center, Montreal Neurological Institute, McGill University, Montreal, QC, Canada; Centre de recherche de l'Institut Universitaire de Gériatrie de Montréal, Montréal, QC, Canada
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.
