The plasticity of the superior longitudinal fasciculus as a function of musical expertise: a diffusion tensor imaging study

Abstract

Previous neuroimaging studies have demonstrated that musical expertise leads to functional alterations in language processing. We utilized diffusion tensor imaging (DTI) to investigate white matter plasticity in musicians with absolute pitch (AP), relative pitch and non-musicians. Using DTI, we analysed the fractional anisotropy (FA) of the superior longitudinal fasciculus (SLF), which is considered the most primary pathway for processing and production of speech and music. In association with different levels of musical expertise, we found that AP is characterized by a greater left than right asymmetry of FA in core fibres of the SLF. A voxel-based analysis revealed three clusters within the left hemisphere SLF that showed significant positive correlations with error rates only for AP-musicians in an AP-test, but not for musicians without AP. We therefore conclude that the SLF architecture in AP musicians is related to AP acuity. In order to reconcile our observations with general aspects of development of fibre bundles, we introduce the Pioneer Axon Thesis, a theoretical approach to formalize axonal arrangements of major white matter pathways.

Keywords: DTI; absolute pitch; language; musical expertise; pioneer axon thesis; plasticity; superior longitudinal fasciculus; white matter.

Figure 1

A 3-D model of the left SLF of a single subject is displayed. The red areas indicate the anterior and posterior ROI used for creating the SLF fibre subset. Only fibres running through both ROIs are considered to be part of the tracked fibre structure.

Figure 2

Here the probability map for the SLF of the AP group (n = 13) is illustrated – combined for two hemispheres. Voxels are displayed with unthresholded probabilities.

Figure 3

The ROIs calculated by thresholding probability maps of bilateral SLFs’ are illustrated in red (left) and blue (right), surrounded by unthresholded group specific probability maps (gold). The bar chart illustrates for each group and both hemispheres the standard deviation (error bars) and means of FA values calculated by comprising all suprathreshold voxels within the defined ROIs (p < 0.05). Asterisks indicate significant inter-hemispheric within-group differences (*p < 0.05) as a result of t-tests for paired samples (two-tailed). Moreover, the between-group analysis (two-way ANOVA) revealed a significant interaction expertise × hemisphere.

Figure 4

The unthresholded probability map of the bilateral SLF served as template to create the illustrated binary mask while performing the voxel-wise analysis.

Figure 5

(A) Shows the three significant clusters (B–D) identified by a voxel-wise multiple regression, characterized by FA values which significantly correlate with the error rates of the APs in the AP-test. The highest correlational effect [designated by the epsilon (ε)] has been identified as the most superior located cluster (B) of the SLF. (B–D) provides close inspections of the significant clusters and plotted correlations obtained by the additional ROI analysis, which is based on the identified clusters in APs (see Section “Materials and Methods”). Accordingly, the error rates are plotted against mean FA values of RP and AP found by the ROI analysis. Asterisks (**p < 0.01) indicate the level of significance with respect to the calculated correlational coefficients (Pearson's r). Furthermore, (B–D) provides additional information concerning the corresponding cluster [k = number of voxels, t = highest t-value within the cluster, (x, y, z) = coordinates of the peak voxel of each cluster in MNI space].

Figure 6

Here a schematic cross-section of the arcuate fasciculus is delineated. On the left (A) the orientation of the fasciculus are defined by three axes anterior–posterior, dorsal–ventral and lateral–medial. The second to the left scheme (B) represents a chaotic distribution of axonal fibres, with several possible arbitrary positions of the pioneer axon, whereas the increased red colour typifies older axonal pathways. The second to the right scheme (C) stands for a possible alternative order driven by a laterally oriented axonal architecture. At the right scheme (D), the proposed architecture due to the maturation of the fasciculus is outlined as suggested by the Pioneer Axon Thesis – thus, the pioneer axon is located medially.

Figure 7

A coronal (A) and a sagittal (B) view of the probability map of the APs’ left SLF are illustrated (blue). The red cluster represents the overlaid ROI (Figure 3) due to the thresholded probability map (p < 0.05), whereas the golden cluster (see also Figure 5B) represents voxels of FA values (−28, −28, 44) that are significantly correlated (r = 0.758**) with the error rates of APs with respect to the AP-test.