Musical training induces functional and structural auditory-motor network plasticity in young adults

Qiongling Li, Xuetong Wang, Shaoyi Wang, Yongqi Xie, Xinwei Li, Yachao Xie, Shuyu Li, Qiongling Li, Xuetong Wang, Shaoyi Wang, Yongqi Xie, Xinwei Li, Yachao Xie, Shuyu Li

Abstract

Playing music requires a strong coupling of perception and action mediated by multimodal integration of brain regions, which can be described as network connections measured by anatomical and functional correlations between regions. However, the structural and functional connectivities within and between the auditory and sensorimotor networks after long-term musical training remain largely uninvestigated. Here, we compared the structural connectivity (SC) and resting-state functional connectivity (rs-FC) within and between the two networks in 29 novice healthy young adults before and after musical training (piano) with those of another 27 novice participants who were evaluated longitudinally but with no intervention. In addition, a correlation analysis was performed between the changes in FC or SC with practice time in the training group. As expected, participants in the training group showed increased FC within the sensorimotor network and increased FC and SC of the auditory-motor network after musical training. Interestingly, we further found that the changes in FC within the sensorimotor network and SC of the auditory-motor network were positively correlated with practice time. Our results indicate that musical training could induce enhanced local interaction and global integration between musical performance-related regions, which provides insights into the mechanism of brain plasticity in young adults.

Keywords: auditory-motor network; brain plasticity; functional connectivity; musical training; structural connectivity.

Conflict of interest statement

The authors declare that there are no conflicts of interest regarding the publication of this article.

© 2018 Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Framework for the investigation. (a) Longitudinal experiment: we used a within‐subject design comprising a training group in which participants received 24‐weeks piano training, and a control group with no intervention. Participants were all tested at 3‐time points: at the beginning (Tp1) and the end (Tp2) of 24 weeks training and at 12 weeks after training (Tp3). At each time point, the participants all received musical assessments, behavioral tests, and scanning sessions. (b) MRI data processing: group ICA was used to acquire the auditory network (AN) and sensorimotor network (SMN) and its corresponding time courses. Probabilistic fiber tracking was conducted to acquire the WM tracts within and between the auditory and sensorimotor cortices: (i) voxel‐wise ANOVA of AN and SMN; (ii) extraction of the time series from the significant clusters; (iii) correlation analysis between the time series of the significant clusters; (iv) extraction of the time courses from group ICA; (v) correlation analysis between the time series of AN and SMN; (vi) thresholded and binarized the WM tracts; (vii) calculation of the mean FA of the pathways within the auditory or sensorimotor regions; (vii) calculation of the mean FA of the pathway between the auditory and sensorimotor regions. Notes: Tp1, time point 1; Tp2, time point 2; Tp3, time point 3; ICA, independent component analysis; AN, auditory network; SMN, sensorimotor network; FC, functional connectivity; SC, structural connectivity; ANOVA, analysis of variance [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 2
Figure 2
The functional auditory network and sensorimotor network. The auditory network and sensorimotor network were identified by group ICA. The AN was formed by the bilateral middle and superior temporal gyrus, and Heschl's gyrus; the SMN was formed by the bilateral precentral/postcentral gyrus and bilateral SMA. Note: AN, auditory network; SMN, sensorimotor network; SMA, supplementary motor area [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 3
Figure 3
Functional connectivity comparisons and correlation analyses. (a) Comparisons showed increased functional connectivity between the right postcentral and right precentral gyri (regions within SMN) when Tp2 (at the end of training) was compared with Tp1 (at the beginning of training) (**p < .001) and decreased functional connectivity when Tp3 (at 12 weeks after training) was compared with Tp2 (*p = .001) in the training group, whereas there was no significant change in the control group. (b) The scatter plot shows that participants in the training group who practiced for longer time showed greater increased functional connectivity (Tp2–Tp1) between right postcentral and precentral gyri ( r2=.395, p<.001). (c) Comparisons showed increased functional connectivity between SMN and AN when Tp2 (at the end of training) was compared with Tp1 (at the beginning of training) (**p < .001), decreased functional connectivity when Tp3 (at 12 weeks after training) was compared with Tp2 (*p = .003), and increased functional connectivity when Tp3 was compared with Tp1 (*p = .02) in the training group, whereas there was no significant change in the control group. (d) No significant correlation was found between the changes of functional connectivity (Tp2–Tp1) between the auditory and sensorimotor cortices and the practice time in the training group ( r2=.045, p=.27). Note: Tp1, time point 1; Tp2, time point 2; Tp3, time point 3; FC, functional connectivity; SMN, sensorimotor network; AN, auditory network
Figure 4
Figure 4
White matter fiber pathway within and between auditory and sensorimotor regions. (a) The WM tracts between auditory and sensorimotor regions were reconstructed by performing probabilistic fiber tracking between two ROI masks (auditory and sensorimotor regions). The two ROIs were connected by the corticospinal tract, superior longitudinal fasciculus, and corpus callosum. (b) The WM tracts within the auditory or sensorimotor regions were reconstructed by performing a probabilistic fiber tracking in which the seed mask and target mask were both the auditory and sensorimotor regions in the AAL template. Note: L, left side of the brain; R, right side of the brain; A, anterior side of the brain; P, posterior side of the brain [Color figure can be viewed at http://wileyonlinelibrary.com]
Figure 5
Figure 5
Structural connectivity comparisons and correlation analysis. (a) Structural connectivity between auditory and sensorimotor regions was evaluated by the mean FA of the WM tracts between the two regions in which probabilistic tracking was obtained. Comparisons showed increased mean FA of the WM tracts between sensorimotor and auditory cortices when Tp2 (at the end of training) was compared with Tp1 (at the beginning of training) (**p < .001) and decreased mean FA when Tp3 (at 12 weeks after training) was compared with Tp2 (**p < .001) in the training group, whereas there was no significant change in the control group. (b) Correlation analysis showed that increased mean FA of the WM tracts (Tp2–Tp1) between sensorimotor and auditory cortices was positively correlated with practice time in the training group ( r2=.370, p<.001). Note: Tp1, time point 1; Tp2, time point 2; Tp3, time point 3; FA, fractional anisotropy; WM, white matter

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