Elsevier

NeuroImage

Volume 59, Issue 4, 15 February 2012, Pages 3364-3372
NeuroImage

Dynamic gray matter changes within cortex and striatum after short motor skill training are associated with their increased functional interaction

https://doi.org/10.1016/j.neuroimage.2011.10.089Get rights and content

Abstract

Gray matter (GM) changes have been described after short learning tasks that lasted for 7 days or after external stimulation that lasted for 5 days. However, the early time course of training-dependent GM changes is still unknown. We investigated whether shorter motor training sessions (four times of 30 min training) would induce GM changes. Therefore, T1-weighted MRIs were acquired daily. Because reported GM changes were induced by learning, a close relationship was assumed between the functional activity and the GM changes. Therefore, fMRI was performed in addition to daily T1-weighted MRIs.

At the end of the four training sessions (at time point “post”), the test results of the trained motor skill were associated with an increase of GM in secondary cortical motor areas (dPMCright, dPMCleft, SMAleft and the right inferior parietal lobule, IPLright). The earliest time point at which a GM change was detected was 1 day before in the right ventral striatum (by contrasting daily T1-weighted MRI vs. baseline). To analyze whether this very early GM change within the right ventral striatum is associated with those GM changes at time point post (which were associated with motor skill performance), their functional connectivity was investigated over the time period of motor skill training. This analysis revealed an increase of functional coupling between these regions (striatum and cortex) over the training days.

The current data demonstrate training-induced short GM plasticity is paralleled by their temporally dynamical process of functional interaction between the cortex and the striatum in response to a motor skill training.

Highlights

► We were interested in the early dynamic time course of gray matter (GM) changes. ► Daily fMRI and T1-MRIs were acquired over a 5-day left-hand-training period. ► Motor skill improvement was associated with GM increase in cortical regions. ► Shortest GM increase was evident within ventral striatum (VS). ► GM increase within VS was functionally linked to GM changes in cortical regions.

Introduction

Rapid gray matter (GM) changes have been observed following repetitive nociceptive input over a period of 8 days (Teutsch et al., 2008), also after visuo-motor training as early as 7 days after commencement of the training (Driemeyer et al., 2008). In addition, shorter time frame (5 days) that induced GM changes were reported following repetitive transcranial magnetic stimulation (May et al., 2007). However, the exact time point of the occurrence of these GM changes is unknown, particularly during training for a motor skill.

Considering the fact that all of the reported GM changes (independent of the time point of occurrence) were training-induced and behaviorally relevant, e.g. (Draganski et al., 2004, Draganski et al., 2006), it seems reasonable to assume that a close relationship exists between these functional and structural changes. An overlap of the GM and functional activation changes in relevant cortical areas while subjects practiced mirror reading over a 14 day period was recently reported (Ilg et al., 2008). To date, no previous experiments have reported the time course of these rapid GM changes or the extent of the association between these GM changes and the parallel, dynamic course of the functional modulation during the time duration of the training. Such a close association would suggest that rapid GM changes are generated by a functional challenge due to a specific task.

To investigate these hypotheses, healthy subjects were trained to perform a specific motor skill (writing their signature with the non-dominant left hand) during four sessions of 30 min per day over a 5-day period (this duration is the shortest reported time period necessary to induce GM changes, see above). The subjects were scanned on a daily basis to capture the initial stages and temporal dynamics of the structural and functional task-related changes and to allow us to investigate the association between the functional and structural changes in the motor network.

Section snippets

Subjects

Twenty-one healthy, right-handed volunteers (11 females, mean age: 23.8 years), according to the Edinburgh handedness inventory (Oldfield, 1971), participated in this study (the final analysis included 16 subjects; see below). These volunteers gave written, informed consent before participating. In addition, this study was approved by the local Ethics Committee.

Experimental protocol

Baseline MRIs (an fMRI and a T1-weighted MRI) were acquired before the first training session, and a baseline test of motor skill

Results

The final analysis included 16 subjects (two subjects were excluded as a result of head movements over greater than 2 mm, and three were excluded as a result of technical EMG recording problems).

Discussion

By the monitoring the functional and structural brain changes that were associated with a motor learning task, we found significant differences that fell into three broad groups:

  • 1.

    The performance improvement of a trained motor skill was associated with an increase of GM in distinct secondary cortical motor areas (IPLright, dPMCleft, dPMCright, and SMAleft) over training days. This occurrence of GM change after a short time period is in agreement with previous findings (May et al., 2007); (Teutsch

Acknowledgments

We are grateful to all of the volunteers who participated in this study. We thank Hansjoerg Mast and Jan Stekelenburg for their support during data acquisition, Franz Aiple for his help using the computer programs and Rumyana Kristeva for her hardware support. This study was partially funded by the European Commission under the 7th Framework Program “Health”, Collaborative Project “Plasticise” (223524).

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