Gray matter volume is associated with rate of subsequent skill learning after a long term training intervention

Abstract

The ability to predict learning performance from brain imaging data has implications for selecting individuals for training or rehabilitation interventions. Here, we used structural MRI to test whether baseline variations in gray matter (GM) volume correlated with subsequent performance after a long-term training of a complex whole-body task. 44 naïve participants were scanned before undertaking daily juggling practice for 6weeks, following either a high intensity or a low intensity training regime. To assess performance across the training period participants' practice sessions were filmed. Greater GM volume in medial occipito-parietal areas at baseline correlated with steeper learning slopes. We also tested whether practice time or performance outcomes modulated the degree of structural brain change detected between the baseline scan and additional scans performed immediately after training and following a further 4weeks without training. Participants with better performance had higher increases in GM volume during the period following training (i.e., between scans 2 and 3) in dorsal parietal cortex and M1. When contrasting brain changes between the practice intensity groups, we did not find any straightforward effects of practice time though practice modulated the relationship between performance and GM volume change in dorsolateral prefrontal cortex. These results suggest that practice time and performance modulate the degree of structural brain change evoked by long-term training regimes.

Keywords: MRI; Skill learning; Structural plasticity.

Copyright © 2014. Published by Elsevier Inc.

Figures

Fig. S1

a) Learning curves for all participants. b) Learning and logarithm curve of a representative participant c) Average performance for all participants. Bars represent standard deviation.

Fig. 1

Average performance score for each group per day. (0: 2 balls; 1: 1 cycle of 3-ball cascade; 2: 2 cycles; 3: 3 cycles; 4: 5–10 s of sustained 3-ball cascade; 5: 10–20 s; 6: 20–30 s; 7: > 30 s; 8: > 60 s; 9: > 60 s and at least one other pattern for  60 s and at least one other pattern for > 60 s). There is a significant effect of day but no significant interaction effect or significant differences between groups. Bars represent standard error.

Fig. 2

Baseline GM volume correlates with subsequent learning rate. a) GM volume in right visual and parietal cortex at baseline correlates with subsequent learning rate. Yellow–red voxels represent significant clusters superimposed on MNI template. Color bar represents t-scores. b) Scatter plot showing the correlation between GM volume averaged across voxels in significant brain areas (shown in 2a) and learning rate for the low intensity group (dark gray symbols) and the high intensity group (black symbols) is displayed for visualization of the range of individual values only and not for inference. c) Regions where GM volume correlates with subsequent learning partly overlap with regions where GM changes with learning in the current study (see Fig. 4c). Yellow cluster corresponds to regions showing significant GM volume change after learning (from Fig. 4c), blue cluster represents regions showing a correlation between GM volume at baseline and learning rate (from Fig. 2a) and green cluster shows the intersection between both clusters. d) GM volume in bilateral DLPFC and SMA correlated with long-term-retention. Yellow–red voxels represent significant clusters superimposed on MNI template. Color bar represents t-scores. Clusters are shown at a corrected cluster extent threshold of p 

Fig. 3

Interaction effect between practice group and average performance, between scan 1 and scan 2. a) Yellow–red voxels correspond to the significant cluster, superimposed on MNI template. Color bar represents t-scores. b) Scatter plot of mean GM change and average performance correlation for the low intensity group (dark gray symbols) and the high intensity group (black symbols) are displayed for visualization of the range of values only and not for inference. Clusters are shown at a corrected cluster extent threshold of p 

Fig. 4

Longer term effects: Scans 1 to 3 and scans 2 to 3. a) GM volume decreases between scans 1 and 3 in the left temporal cortex, insula and operculum. Blue–dark blue voxels correspond to the significant clusters. b) Mean GM values of the blue clusters throughout time relative to scan 1. c) GM volume increases between scans 2 and 3 in the visual and parietal cortex (Yellow–red voxels). d) Mean GM values of the yellow–red clusters at different time points relative to scan 1. e) GM volume decreases between scans 2 and 3 in the superior temporal gyrus, insula and operculum (Blue–dark blue voxels). f) Mean GM values of the blue clusters throughout time relative to scan 1. Plots are for illustrative purposes only and not for inference. Error bars represent standard error. Clusters are superimposed on MNI template. Color bars represent t-scores. Clusters are shown at a corrected cluster extent threshold of p 

Fig. 5

Participants with better performance have higher GM increases during the follow-up period. a) Cluster's mean GM change values correlation with the average performance after the learning period (between scans 2 and 3). b) Correlation plot between the average performance and GM change in a) is displayed for visualization of the range of individual values and not for inference. Color bar represents t-scores. Clusters are shown at a corrected cluster extent threshold of p