Functional and Structural Plasticity Co-express in a Left Premotor Region During Early Bimanual Skill Learning.

Friederike Irmen,Anke Ninija Karabanov,Kasper Winther Andersen,Kristoffer Hougaard Madsen,Hartwig Roman Siebner,Thue Bisgaard,Sophie Alida Bögemann,Tim B Dyrby

doi:10.3389/fnhum.2020.00310

Abstract

Introduction: Motor skill learning already triggers the functional reorganization of regional brain activity after short periods of training. Recent studies suggest that microstructural change may emerge at similar timescales, but the spatiotemporal profiles of functional and structural plasticity have rarely been traced in parallel. Recently, we demonstrated that 5 days of endoscopic skill training induces changes in task-related brain activity in the ventral premotor cortex (PMv) and other areas of the frontoparietal grasping network. Here, we analyzed microstructural data, collected during the same experiment to investigate if microstructural plasticity overlaps temporally and spatially with the training-induced changes in task-related brain activity.Materials and Methods: Thirty-nine students were divided into a full-routine group (n = 20), that underwent three endoscopy training sessions in the MR-scanner as well as a 5-day virtual reality (VR)-endoscopy training and a brief-routine group (n = 19), that only performed the in-scanner endoscopy training sessions. Diffusion Tensor Imaging (DTI)-derived fractional anisotropy (FA) and resting-state functional magnetic resonance imaging (rs-fMRI) were collected at baseline, after the first and after the last VR-training session.Results: The full-routine group showed significant FA changes in a left-hemispheric subcortical cluster underlying the PMv region, for which we previously demonstrated functional plasticity during endoscopy training in the same sample. Functional (task-related fMRI) and structural (FA) changes showed the largest change from the first to the second scan, suggesting similar temporal dynamics. In the full-routine group, the FA change in the subcortical cluster underlying the left PMv scaled positively with the individual improvement in endoscopic surgery.Conclusion: Microstructural white-matter plasticity mirrors the spatiotemporal profile of task-dependent plasticity during a 5-day course of endoscopy skill training. The observed similarities motivate future research on the interplay between functional and structural plasticity during early skill acquisition.

Highlights

Motor skill learning already triggers the functional reorganization of regional brain activity after short periods of training
For the full-routine group, a significant decrease in Fractional Anisotropy (FA) in the left superior longitudinal fasciculus (SLF) precentral white matter was detected from Day 0 to Day 1 (58 voxels, peak-level MNI coordinates: x = −39, y = −11, z = 28, tmax = 2.74 and pFWEcorr = 0.03, Figures 2A,B)
No change could be observed in the brief-routine group. Both mean diffusivity (MD) and AD decreased slightly, not significantly; and there was a trending increase in RD from Day 0 to Day 1 close to the region where FA was significantly changed (34 voxels, peak-level MNI coordinates: x = −36, y = −12, z = 26, tmax = −1.63, p = 0.06)

Summary

Introduction

Motor skill learning already triggers the functional reorganization of regional brain activity after short periods of training. We demonstrated that 5 days of endoscopic skill training induces changes in task-related brain activity in the ventral premotor cortex (PMv) and other areas of the frontoparietal grasping network. This trajectory is associated with characteristic changes in brain activity: during early learning, neuronal activity increases in sensorimotor areas, which is typically followed by a ‘‘pruning’’ of activity at later learning stages (Dayan and Cohen, 2011; Ma et al, 2011; Makino et al, 2017). We demonstrated task-dependent activity increases at early learning stages in the frontoparietal grasping network during bimanual skill learning (Karabanov et al, 2019). During the three in-scanner endoscopy sessions both groups showed an activity increase in the left frontoparietal grasping pathway but only in the full-routine group, the changes were accompanied by a similar activity increase in the right frontoparietal grasping network and a modulation of bilateral premotor connectivity (Karabanov et al, 2019)

Methods

Results

Conclusion