Brain changes following four weeks of unimanual motor training: Evidence from fMRI‐guided diffusion MRI tractography

Reid, Lee B.; Sale, Martin V.; Cunnington, Ross; Mattingley, Jason B.; Rose, Stephen

doi:10.1002/hbm.23514

Cited by 36 publications

(70 citation statements)

References 42 publications

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“…Although transfer of skill did occur, both between sequences and between hands, our fMRI and TMS analyses were not explicitly designed to investigate such effects. Diffusion MRI analyses detailed in a companion paper 224 explored transfer effects in the same participant group in more detail.…”

Section: Discussionmentioning

confidence: 99%

“…The third possibility, regarding changes in white matter, is investigated in detail in our followup publication. 224 …”

Section: Tmsmentioning

confidence: 99%

“…181 The dlPFC and related areas were further investigated with diffusion imaging; these analyses are described in a separate publication. 224 …”

Section: Cortical Thicknessmentioning

confidence: 99%

“…Findings from a fifth measure, diffusion MRI, appear in a second study. 224 Each of these modalities helps to build a global picture of the changes that occur with motor training, by reporting on a slightly different aspect of the neuroplastic response.…”

Section: Introductionmentioning

confidence: 99%

“…Finally, we tested for increased cortical thickness in motor areas of the trained hemisphere, given reports of subtle changes in visuomotor areas associated with visuomotor learning. 52,80,223 In combination with our parallel analysis of white matter and network changes, 224 this work provides a comprehensive assessment of the functional and structural brain changes associated with motor learning in humans.…”

Section: Introductionmentioning

confidence: 99%

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Measuring motor-training induced neuroplasticity using diffusion and functional MRI: a sensitive, pathology-robust approach

Reid¹

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Brain injury constitutes a significant health burden worldwide, and outcomes are generally poor. To improve treatment, we must better understand how injury affects brain function, how the brain responds to learning pressures (neuroplasticity), and the interaction between the two. This is difficult, however, because of current technological shortcomings.This thesis focusses on the measurement of neuroplasticity in response to motor training in situations such as rehabilitation following brain injury. Although the principles and methods discussed generalise to many forms of brain pathology, discussion is generally focussed on unilateral cerebral palsy (UCP) because altered brain-development in UCP makes analyses particularly difficult. This begins with a literature review (Chapter 2) that outlines UCP, rehabilitative approaches, and the relationship between atypical brain organisation and early-life brain injury. Also discussed is how novel rehabilitation strategies may stem from studying brain changes induced by rehabilitation, and why the most informative findings are likely to come from studies utilising multiple imaging modalities.Blood Oxygen-Level Dependent Functional Magnetic Resonance Imaging (fMRI) measures brain activity indirectly and has been used to study neuroplasticity in both healthy participants and those with brain pathology. Although fMRI confounds are well understood, no published work has explored their cumulative effect when brain injury is present. Resultantly, confounds have largely been ignored, leading to heterogeneous findings that have provided little toward understanding brain changes, biologically speaking. Chapter 3 examines the cumulative effect of fMRI confounds, assumptions, and other issues, when attempting to measure neuroplasticity in participants with brain injury. This work concludes that, although fMRI can be expected to locate approximate regions of brain activation in an individual scan, numerous confounding factors make its interpretation, in terms of neuroplasticity, difficult without additional information acquired through alternative means.Diffusion MRI (dMRI) is an imaging modality that is typically used to identify the brain's white-matter pathways and calculate metrics that are influenced by factors such as myelination or axonal density. Standard dMRI analyses are ill suited to studying brain injury due to their reliance on brain 'atlases' which indicate relationships between brain regions and brain functions. Brain pathology can prevent reliable atlas registration, and alter relationships between structure and function. Chapter 4 details a novel dMRI analysis designed to measure neuroplasticity, addressing the need for a sensitive and reliable alternative to standalone-fMRI. This method utilises surface-based fMRI analyses, rather than brain atlases, to locate regions involved in motor execution. Corticospinal (CST) and thalamocortical tracts emanating from these regions are delineated using dMRI tractography and iii machine learning. This method was app...

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Section: Discussionmentioning

confidence: 99%

“…The third possibility, regarding changes in white matter, is investigated in detail in our followup publication. 224 …”

Section: Tmsmentioning

confidence: 99%

“…181 The dlPFC and related areas were further investigated with diffusion imaging; these analyses are described in a separate publication. 224 …”

Section: Cortical Thicknessmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Measuring motor-training induced neuroplasticity using diffusion and functional MRI: a sensitive, pathology-robust approach

Reid¹

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Brain changes following four weeks of unimanual motor training: Evidence from behavior, neural stimulation, cortical thickness, and functional MRI

et al. 2017

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Although different aspects of neuroplasticity can be quantified with behavioral probes, brain stimulation, and brain imaging assessments, no study to date has combined all these approaches into one comprehensive assessment of brain plasticity. Here, 24 healthy right-handed participants practiced a sequence of finger-thumb opposition movements for 10 min each day with their left hand. After 4 weeks, performance for the practiced sequence improved significantly (P < 0.05 FWE) relative to a matched control sequence, with both the left (mean increase: 53.0% practiced, 6.5% control) and right (21.0%; 15.8%) hands. Training also induced significant (cluster p-FWE < 0.001) reductions in functional MRI activation for execution of the trained sequence, relative to the control sequence. These changes were observed as clusters in the premotor and supplementary motor cortices (right hemisphere, 301 voxel cluster; left hemisphere 700 voxel cluster), and sensorimotor cortices and superior parietal lobules (right hemisphere 864 voxel cluster; left hemisphere, 1947 voxel cluster). Transcranial magnetic stimulation over the right ("trained") primary motor cortex yielded a 58.6% mean increase in a measure of motor evoked potential amplitude, as recorded at the left abductor pollicis brevis muscle. Cortical thickness analyses based on structural MRI suggested changes in the right precentral gyrus, right post central gyrus, right dorsolateral prefrontal cortex, and potentially the right supplementary motor area. Such findings are consistent with LTP-like neuroplastic changes in areas that were already responsible for finger sequence execution, rather than improved recruitment of previously nonutilized tissue. Hum Brain Mapp 38:4773-4787, 2017. © 2017 Wiley Periodicals, Inc.

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Neurite orientation dispersion and density imaging quantifies corticospinal tract microstructural organization in children with unilateral cerebral palsy

Nemanich

Mueller

Gillick

2019

Human Brain Mapping

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Children with unilateral cerebral palsy (UCP) due to early brain injury exhibit disrupted connectivity of corticospinal tracts (CSTs), which can be quantified using diffusion-weighted magnetic resonance imaging (DWI). Diffusion tensor imaging (DTI) is commonly used to quantify white matter organization, however, this model lacks the biological specificity to accurately describe underlying microstructural properties. Newer approaches, such as neurite orientation dispersion and density imaging (NODDI), may provide more biologically accurate information regarding CST microstructure. In this study, we directly compared metrics of CST microstructure using NODDI and DTI models to characterize the microstructural organization of corticospinal pathways. Twenty participants with UCP participating in a neuromodulation/rehabilitation intervention underwent imaging including multi-shell DWI; 10 participants’ datasets were adequately completed for neuroimaging analysis. Task fMRI-guided probabilistic tractography from motor cortex to brainstem was performed at baseline and follow-up to reconstruct the CSTs. Diffusion metrics were compared between hemispheres at baseline, and between baseline and follow-up to test for intervention effects. Correlation analyses were used to compare baseline metrics to changes in hand function following the intervention. DTI results showed that mean fractional anisotropy in lesioned and nonlesioned CSTs did not significantly differ, but mean, axial, and radial diffusivity were greater in the lesioned CST. For NODDI, intracellular volume fraction (ICVF) and orientation dispersion index (ODI) were lower in the lesioned CST. Unimanual function was strongly correlated with ICVF, but not FA. NODDI may reveal distinct properties of CST microstructure that are linked to motor function, indicating their potential in characterizing brain structure and development.

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Brain changes following four weeks of unimanual motor training: Evidence from fMRI‐guided diffusion MRI tractography

Cited by 36 publications

References 42 publications

Measuring motor-training induced neuroplasticity using diffusion and functional MRI: a sensitive, pathology-robust approach

Measuring motor-training induced neuroplasticity using diffusion and functional MRI: a sensitive, pathology-robust approach

Brain changes following four weeks of unimanual motor training: Evidence from behavior, neural stimulation, cortical thickness, and functional MRI

Neurite orientation dispersion and density imaging quantifies corticospinal tract microstructural organization in children with unilateral cerebral palsy

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