Structural and functional brain changes following four weeks of unimanual motor training: evidence from fMRI-guided diffusion MRI tractography

We have reported reliable changes in behaviour, brain structure and function in 24 healthy right-handed adults who practiced a finger-thumb opposition sequence task with their left hand for 10 mins daily, over four weeks. Here we extend these findings by employing diffusion MRI to investigate white-matter changes in the corticospinal tract, basal-ganglia, and connections of the dorsolateral prefrontal cortex. Twenty-three participant datasets were available with pre-training and post-training scans. Task performance improved in all participants (mean: 52.8%, SD: 20.0%; group p<0.01 FWE) and widespread microstructural changes were detected across the motor system of the ‘trained’ hemisphere. Specifically, region-of-interest based analyses of diffusion MRI (n=21) revealed significantly increased fractional anisotropy in the right caudate nucleus (4.9%; p<0.05 FWE), and decreased mean diffusivity in the left nucleus accumbens (-1.3%; p<0.05 FWE). Diffusion MRI tractography (n=22), seeded by sensorimotor cortex fMRI activation, also revealed increased fractional anisotropy in the right corticomotor tract (mean 3.28%; p<0.05 FWE) predominantly reflecting decreased radial diffusivity. These changes were consistent throughout the entire length of the tract. The left corticomotor tract did not show any changes. FA also increased in white matter connections between the right middle frontal gyrus and both right caudate nucleus (17/22 participants; p<0.05 FWE) and right supplementary motor area (18/22 participants; p<0.05 FWE). Equivalent changes in FA were not seen in the left (‘non-trained’) hemisphere. In combination with our functional and structural findings, this study provides detailed, multifocal evidence for widespread neuroplastic changes in the human brain resulting from motor training.

[1]  S. Rose,et al.  Assessment of the structural brain network reveals altered connectivity in children with unilateral cerebral palsy due to periventricular white matter lesions , 2014, NeuroImage: Clinical.

[2]  Henry H Yin,et al.  Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum , 2006, Proceedings of the National Academy of Sciences.

[3]  Celine Mateo,et al.  Motor Control by Sensory Cortex , 2010, Science.

[4]  R. E. Hicks,et al.  Cognitive and Motor Components of Bilateral Transfer , 1983 .

[5]  Derek K. Jones,et al.  The effect of filter size on VBM analyses of DT-MRI data , 2005, NeuroImage.

[6]  Barbara Arrowsmith-Young Plenary 2 – The woman who changed her brain , 2013 .

[7]  Jae Min Lee,et al.  CST recovery in pediatric hemiplegic patients: Diffusion tensor tractography study , 2013, Neuroscience Letters.

[8]  Ross Cunnington,et al.  Interpreting Intervention Induced Neuroplasticity with fMRI: The Case for Multimodal Imaging Strategies , 2015, Neural plasticity.

[9]  L. Cohen,et al.  Neuroplasticity Subserving Motor Skill Learning , 2011, Neuron.

[10]  C. Jack,et al.  Alzheimer's Disease Neuroimaging Initiative , 2008 .

[11]  Ross Cunnington,et al.  Surface-Based fMRI-Driven Diffusion Tractography in the Presence of Significant Brain Pathology: A Study Linking Structure and Function in Cerebral Palsy , 2016, PloS one.

[12]  R. Schachar,et al.  Dissociation of response inhibition and performance monitoring in the stop signal task using event‐related fMRI , 2007, Human brain mapping.

[13]  Anatol C. Kreitzer,et al.  Plasticity in gray and white: neuroimaging changes in brain structure during learning , 2012, Nature Neuroscience.

[14]  J. B. Preston,et al.  Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe , 1994, The Journal of comparative neurology.

[15]  Samuel Bernard,et al.  Dynamics of Oligodendrocyte Generation and Myelination in the Human Brain , 2014, Cell.

[16]  Sébastien Ourselin,et al.  Fast free-form deformation using graphics processing units , 2010, Comput. Methods Programs Biomed..

[17]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

[18]  J. Yates,et al.  Extremely Long-Lived Nuclear Pore Proteins in the Rat Brain , 2012, Science.

[19]  Alan Connelly,et al.  MRtrix: Diffusion tractography in crossing fiber regions , 2012, Int. J. Imaging Syst. Technol..

[20]  Klaus H. Maier-Hein,et al.  Methodological considerations on tract-based spatial statistics (TBSS) , 2014, NeuroImage.

[21]  Pierrick Coupé,et al.  volBrain: An Online MRI Brain Volumetry System , 2015, Front. Neuroinform..

[22]  J. Mattingley,et al.  Structural and functional brain changes following four weeks of unimanual motor training: evidence from behaviour, neural stimulation, cortical thickness and functional MRI , 2016, bioRxiv.

[23]  Paul M. Thompson,et al.  Improved DTI registration allows voxel-based analysis that outperforms Tract-Based Spatial Statistics , 2014, NeuroImage.

[24]  Lutz Jäncke,et al.  Longitudinal reliability of tract‐based spatial statistics in diffusion tensor imaging , 2014, Human brain mapping.

[25]  L. Reid,et al.  Motor pathway degeneration in young ataxia telangiectasia patients: A diffusion tractography study , 2015, NeuroImage: Clinical.

[26]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[27]  Jonathan D. Power,et al.  Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high‐motion data points , 2014, Human brain mapping.

[28]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[29]  B. Stankoff,et al.  Induction of myelination in the central nervous system by electrical activity. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Helgerud,et al.  Structural brain changes after 4 wk of unilateral strength training of the lower limb. , 2013, Journal of applied physiology.

[31]  Luis Augusto Teixeira,et al.  Timing and Force Components in Bilateral Transfer of Learning , 2000, Brain and Cognition.

[32]  Arno Villringer,et al.  Dynamic Properties of Human Brain Structure: Learning-Related Changes in Cortical Areas and Associated Fiber Connections , 2010, The Journal of Neuroscience.

[33]  S. Ionta,et al.  Understanding the role of the primary somatosensory cortex: Opportunities for rehabilitation , 2015, Neuropsychologia.

[34]  Hugh Garavan,et al.  Automaticity and Reestablishment of Executive ControlAn fMRI Study , 2006, Journal of Cognitive Neuroscience.

[35]  Steven L Jones,et al.  Axon Initial Segment Cytoskeleton: Architecture, Development, and Role in Neuron Polarity , 2016, Neural plasticity.

[36]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[37]  Adam G. Thomas,et al.  Functional but not structural changes associated with learning: An exploration of longitudinal Voxel-Based Morphometry (VBM) , 2009, NeuroImage.

[38]  G. B. Pike,et al.  MRI‐based myelin water imaging: A technical review , 2015, Magnetic resonance in medicine.

[39]  Yongmin Chang,et al.  Reorganization and plastic changes of the human brain associated with skill learning and expertise , 2014, Front. Hum. Neurosci..

[40]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[41]  K. Gurney,et al.  The nucleus accumbens as a nexus between values and goals in goal-directed behavior: a review and a new hypothesis , 2013, Front. Behav. Neurosci..

[42]  Daniel C. Alexander,et al.  NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain , 2012, NeuroImage.

[43]  Alan Connelly,et al.  SIFT2: Enabling dense quantitative assessment of brain white matter connectivity using streamlines tractography , 2015, NeuroImage.

[44]  R. Fields,et al.  Astrocytes Promote Myelination in Response to Electrical Impulses , 2006, Neuron.

[45]  Pierrick Coupé,et al.  Automatic thalamus and hippocampus segmentation from MP2RAGE: comparison of publicly available methods and implications for DTI quantification , 2016, International Journal of Computer Assisted Radiology and Surgery.

[46]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[47]  Stephen E. Rose,et al.  Diffusion MRI of the neonate brain: acquisition, processing and analysis techniques , 2012, Pediatric Radiology.