Imaging functional neuroplasticity in human white matter tracts

Tory O Frizzell,Xiaowei Song,Lukas A Grajauskas,Elisha Phull,Ryan C N D'Arcy,Jodie Gawryluk,Mishaa Khan

doi:10.1007/s00429-021-02407-4

Abstract

Magnetic resonance imaging (MRI) studies are sensitive to biological mechanisms of neuroplasticity in white matter (WM). In particular, diffusion tensor imaging (DTI) has been used to investigate structural changes. Historically, functional MRI (fMRI) neuroplasticity studies have been restricted to gray matter, as fMRI studies have only recently expanded to WM. The current study evaluated WM neuroplasticity pre–post motor training in healthy adults, focusing on motor learning in the non-dominant hand. Neuroplasticity changes were evaluated in two established WM regions-of-interest: the internal capsule and the corpus callosum. Behavioral improvements following training were greater for the non-dominant hand, which corresponded with MRI-based neuroplasticity changes in the internal capsule for DTI fractional anisotropy, fMRI hemodynamic response functions, and low-frequency oscillations (LFOs). In the corpus callosum, MRI-based neuroplasticity changes were detected in LFOs, DTI, and functional correlation tensors (FCT). Taken together, the LFO results converged as significant amplitude reductions, implicating a common underlying mechanism of optimized transmission through altered myelination. The structural and functional neuroplasticity findings open new avenues for direct WM investigations into mapping connectomes and advancing MRI clinical applications.

Highlights

The human brain is a dynamic and highly integrated system with a dense array of connections, which in essence, allows for performance of tasks and behavioral change
Significant LH > RH differences were present for functional correlation tensors (FCT) in the corpus callosum (Fig. 2, panel B)
White matter (WM) functional MRI (fMRI) activity was embedded within a wider network of distributed gray matter (GM) fMRI activity (Supplemental Fig. 1)

Summary

Introduction

The human brain is a dynamic and highly integrated system with a dense array of connections, which in essence, allows for performance of tasks and behavioral change. WM changes are experience-dependent and have been well established as a critical contributing aspect of neuroplasticity in the adult brain (Sampaio-Baptista and Johansen-Berg 2017; Fields 2011). Activitydependent regulation of myelin through oligodendrocytes and oligodendrocyte-precursor cells appear to play an important role in both structural and functional neuroplasticity (Sampaio-Baptista and Johansen-Berg 2017; Foster et al 2019). For instance, experience-dependent WM neuroplasticity alters structural axon properties, such as myelin, axon diameter, and internode length, leading to functional and physiological changes such as conduction speed (Fields 2015; Sampaio-Baptista and Johansen-Berg 2017). The first MRI investigation of experiencedependent changes in WM was published by Scholz et al (2009), who demonstrated diffusion tensor imaging (DTI)

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