White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response Variability

Numerous studies have noted the importance of white matter changes in motor learning, but existing literature only focuses on structural and microstructural MRI changes, as there are limited tools available for in vivo investigations of white matter function. One method that has gained recent promin...

Full description

Bibliographic Details
Main Authors: Tory O. Frizzell, Lukas A. Grajauskas, Careesa C. Liu, Sujoy Ghosh Hajra, Xiaowei Song, Ryan C. N. D’Arcy
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-10-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnhum.2020.509258/full
id doaj-1b2f811c1bec4dcb88145d5cc529999c
record_format Article
collection DOAJ
language English
format Article
sources DOAJ
author Tory O. Frizzell
Tory O. Frizzell
Lukas A. Grajauskas
Lukas A. Grajauskas
Lukas A. Grajauskas
Careesa C. Liu
Careesa C. Liu
Careesa C. Liu
Sujoy Ghosh Hajra
Sujoy Ghosh Hajra
Sujoy Ghosh Hajra
Xiaowei Song
Xiaowei Song
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
spellingShingle Tory O. Frizzell
Tory O. Frizzell
Lukas A. Grajauskas
Lukas A. Grajauskas
Lukas A. Grajauskas
Careesa C. Liu
Careesa C. Liu
Careesa C. Liu
Sujoy Ghosh Hajra
Sujoy Ghosh Hajra
Sujoy Ghosh Hajra
Xiaowei Song
Xiaowei Song
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response Variability
Frontiers in Human Neuroscience
functional magnetic resonance imaging
white matter activation
neuroplasticity
motor learning
functional connectivity
internal capsule
author_facet Tory O. Frizzell
Tory O. Frizzell
Lukas A. Grajauskas
Lukas A. Grajauskas
Lukas A. Grajauskas
Careesa C. Liu
Careesa C. Liu
Careesa C. Liu
Sujoy Ghosh Hajra
Sujoy Ghosh Hajra
Sujoy Ghosh Hajra
Xiaowei Song
Xiaowei Song
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
Ryan C. N. D’Arcy
author_sort Tory O. Frizzell
title White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response Variability
title_short White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response Variability
title_full White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response Variability
title_fullStr White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response Variability
title_full_unstemmed White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response Variability
title_sort white matter neuroplasticity: motor learning activates the internal capsule and reduces hemodynamic response variability
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2020-10-01
description Numerous studies have noted the importance of white matter changes in motor learning, but existing literature only focuses on structural and microstructural MRI changes, as there are limited tools available for in vivo investigations of white matter function. One method that has gained recent prominence is the application of blood oxygen level dependent (BOLD) fMRI to white matter, with high-field scanners now being able to better detect the smaller hemodynamic changes present in this tissue type compared to those in the gray matter. However, fMRI techniques have yet to be applied to investigations of neuroplastic change with motor learning in white matter. White matter function represents an unexplored component of neuroplasticity and is essential for gaining a complete understanding of learning-based changes occurring throughout the whole brain. Twelve healthy, right-handed participants completed fine motor and gross motor tasks with both hands, using an MRI compatible computer mouse. Using a crossover design along with a prior analysis approach to establish WM activation, participants received a baseline scan followed by 2 weeks of training, returning for a midpoint and endpoint scan. The motor tasks were designed to be selectively difficult for the left hand, leading to a training effect only in that condition. Analysis targeted the comparison and detection of training-associated right vs left hand changes. A statistically significant improvement in motor task score was only noted for the left-hand motor condition. A corresponding change in the temporal characteristics of the white matter hemodynamic response was shown within only the right corticospinal tract. The hemodynamic response exhibited a reduction in the dispersion characteristics after the training period. To our knowledge, this is the first report of MRI detectable functional neuroplasticity in white matter, suggesting that modifications in temporal characteristics of white matter hemodynamics may underlie functional neuroplasticity in this tissue.
topic functional magnetic resonance imaging
white matter activation
neuroplasticity
motor learning
functional connectivity
internal capsule
url https://www.frontiersin.org/articles/10.3389/fnhum.2020.509258/full
work_keys_str_mv AT toryofrizzell whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT toryofrizzell whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT lukasagrajauskas whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT lukasagrajauskas whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT lukasagrajauskas whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT careesacliu whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT careesacliu whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT careesacliu whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT sujoyghoshhajra whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT sujoyghoshhajra whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT sujoyghoshhajra whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT xiaoweisong whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT xiaoweisong whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT ryancndarcy whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT ryancndarcy whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT ryancndarcy whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
AT ryancndarcy whitematterneuroplasticitymotorlearningactivatestheinternalcapsuleandreduceshemodynamicresponsevariability
_version_ 1724533053410246656
spelling doaj-1b2f811c1bec4dcb88145d5cc529999c2020-11-25T03:40:44ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612020-10-011410.3389/fnhum.2020.509258509258White Matter Neuroplasticity: Motor Learning Activates the Internal Capsule and Reduces Hemodynamic Response VariabilityTory O. Frizzell0Tory O. Frizzell1Lukas A. Grajauskas2Lukas A. Grajauskas3Lukas A. Grajauskas4Careesa C. Liu5Careesa C. Liu6Careesa C. Liu7Sujoy Ghosh Hajra8Sujoy Ghosh Hajra9Sujoy Ghosh Hajra10Xiaowei Song11Xiaowei Song12Ryan C. N. D’Arcy13Ryan C. N. D’Arcy14Ryan C. N. D’Arcy15Ryan C. N. D’Arcy16Simon Fraser University ImageTech Lab, Health Science and Innovation, Surrey Memorial Hospital, Fraser Health, Surrey, BC, CanadaFaculty of Applied Sciences, Simon Fraser University, Burnaby, BC, CanadaSimon Fraser University ImageTech Lab, Health Science and Innovation, Surrey Memorial Hospital, Fraser Health, Surrey, BC, CanadaCumming School of Medicine, University of Calgary, Calgary, AB, CanadaDepartment of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, CanadaSimon Fraser University ImageTech Lab, Health Science and Innovation, Surrey Memorial Hospital, Fraser Health, Surrey, BC, CanadaFaculty of Applied Sciences, Simon Fraser University, Burnaby, BC, CanadaRotman Research Institute, Baycrest Health Sciences, Toronto, ON, CanadaSimon Fraser University ImageTech Lab, Health Science and Innovation, Surrey Memorial Hospital, Fraser Health, Surrey, BC, CanadaFaculty of Applied Sciences, Simon Fraser University, Burnaby, BC, CanadaFlight Research Laboratory, National Research Council Canada, Ottawa, ON, CanadaSimon Fraser University ImageTech Lab, Health Science and Innovation, Surrey Memorial Hospital, Fraser Health, Surrey, BC, CanadaDepartment of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, CanadaSimon Fraser University ImageTech Lab, Health Science and Innovation, Surrey Memorial Hospital, Fraser Health, Surrey, BC, CanadaFaculty of Applied Sciences, Simon Fraser University, Burnaby, BC, CanadaDepartment of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, CanadaDjavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, BC, CanadaNumerous studies have noted the importance of white matter changes in motor learning, but existing literature only focuses on structural and microstructural MRI changes, as there are limited tools available for in vivo investigations of white matter function. One method that has gained recent prominence is the application of blood oxygen level dependent (BOLD) fMRI to white matter, with high-field scanners now being able to better detect the smaller hemodynamic changes present in this tissue type compared to those in the gray matter. However, fMRI techniques have yet to be applied to investigations of neuroplastic change with motor learning in white matter. White matter function represents an unexplored component of neuroplasticity and is essential for gaining a complete understanding of learning-based changes occurring throughout the whole brain. Twelve healthy, right-handed participants completed fine motor and gross motor tasks with both hands, using an MRI compatible computer mouse. Using a crossover design along with a prior analysis approach to establish WM activation, participants received a baseline scan followed by 2 weeks of training, returning for a midpoint and endpoint scan. The motor tasks were designed to be selectively difficult for the left hand, leading to a training effect only in that condition. Analysis targeted the comparison and detection of training-associated right vs left hand changes. A statistically significant improvement in motor task score was only noted for the left-hand motor condition. A corresponding change in the temporal characteristics of the white matter hemodynamic response was shown within only the right corticospinal tract. The hemodynamic response exhibited a reduction in the dispersion characteristics after the training period. To our knowledge, this is the first report of MRI detectable functional neuroplasticity in white matter, suggesting that modifications in temporal characteristics of white matter hemodynamics may underlie functional neuroplasticity in this tissue.https://www.frontiersin.org/articles/10.3389/fnhum.2020.509258/fullfunctional magnetic resonance imagingwhite matter activationneuroplasticitymotor learningfunctional connectivityinternal capsule