Motor Skill Learning Induces Changes in White Matter Microstructure and Myelination

Abstract

Learning a novel motor skill is associated with well characterized structural and functional plasticity in the rodent motor cortex. Furthermore, neuroimaging studies of visuomotor learning in humans have suggested that structural plasticity can occur in white matter (WM), but the biological basis for such changes is unclear. We assessed the influence of motor skill learning on WM structure within sensorimotor cortex using both diffusion MRI fractional anisotropy (FA) and quantitative immunohistochemistry. Seventy-two adult (male) rats were randomly assigned to one of three conditions (skilled reaching, unskilled reaching, and caged control). After 11 d of training, postmortem diffusion MRI revealed significantly higher FA in the skilled reaching group compared with the control groups, specifically in the WM subjacent to the sensorimotor cortex contralateral to the trained limb. In addition, within the skilled reaching group, FA across widespread regions of WM in the contralateral hemisphere correlated significantly with learning rate. Immunohistological analysis conducted on a subset of 24 animals (eight per group) revealed significantly increased myelin staining in the WM underlying motor cortex in the hemisphere contralateral (but not ipsilateral) to the trained limb for the skilled learning group versus the control groups. Within the trained hemisphere (but not the untrained hemisphere), myelin staining density correlated significantly with learning rate. Our results suggest that learning a novel motor skill induces structural change in task-relevant WM pathways and that these changes may in part reflect learning-related increases in myelination.

The dynamics of cortical GABA in human motor learning

“…Specifically, evidence from both human and non-human primate studies suggests that repeated prac ce of a motor skill is associated with changes in the topographic organisa on of the region (Nudo et al, 1996;Karni et al, 1998). Further, the learning of fine motor skills has been associated with synaptogenesis in M1 (Kleim et al, 2002), as well as changes in the myelina on of the underlying white ma er (Sampaio-Bap sta et al, 2013). Understanding the physiological processes that drive the observed structural and func onal changes in M1 to support motor learning are necessary for the development of therapeu c approaches to promote adap ve plas city a er brain injuries, such as stroke, via facilita on of the re-learning of motor skills compromised by brain pathology.…”

A common brain network links development, aging, and vulnerability to disease

“…Although structural MRI does not distinguish between the various cellular mechanisms underpinning development and aging processes [e.g., dendritic and synaptic remodeling, neurogenesis and neuronal death, astrogliosis, (de)myelination], this technique is sensitive to detect the overall contribution of these mechanisms to macroscopic age-related changes in brain structure (8)(9)(10).…”

Studying neuroanatomy using MRI

“…Such alterations could be detected within a day and yet seemed to last for weeks or months 66 . At the level of correlations, diffusion properties changes in white matter were correlated with myelin markers 67 ; diffusion in grey matter correlated with astrocytic and synaptic markers 65 . Volumetric changes similarly correlated with synaptic markers, in particular GAP43, an axonal growth cone indicator 64,68 , dendritic spine counts 69 , and glutamate concentration 70 .…”