White matter integrity of motor tracts in professional
musicians and soccer players
Poster No.:
C-1431
Congress:
ECR 2013
Type:
Scientific Exhibit
Authors:
D. Kaufmann , I. Koerte , M. Muehlmann , E. Hartl , M. F. Reiser ,
1
2
1
2
1
2
1
1
1 1
N. Makris , Y. Rathi , M. Shenton , B. Ertl-Wagner ; Munich/DE,
2
Boston, MA/US
Keywords:
Neuroradiology brain, MR-Diffusion/Perfusion, Comparative
studies
DOI:
10.1594/ecr2013/C-1431
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Page 1 of 12
Purpose
The aim of this study was to characterize white matter (WM) integrity in professional
musicians compared to professional soccer players using advanced MR diffusion tensor
imaging (DTI) techniques.
Methods and Materials
Participants
Sixteen male professional musicians (24.8 ± 2.4 years of age) and seventeen age- and
gender-matched professional soccer players from soccer clubs in Germany (24.4 ± 2.5
years of age) were included in the study. All subjects were right-handed and practiced for
their profession since childhood. The mean total duration of playing soccer was 18.8 ± 2.6
years (10.1 ± 4.1 hours of training per week). Musicians played instruments that require
sequential finger movements such as the piano, the guitar, the bass guitar and the cello.
The mean total duration of playing an instrument in the musicians group was 15.4 ± 3.2
years (11.3 ± 8.4 hours of training per week). None of the participants had a documented
history of any neurological or psychiatric disease. None of the musicians played soccer
on a regular basis and none of the soccer player played any musical instrument.
MR imaging protocol
All data were acquired on a 3T MR scanner with a 12-channel head coil array. Anatomical
sequences consisted of 3D magnetization prepared rapid-acquisition gradient echo (MPRAGE) acquired in a sagittal orientation and motion insensitive 3D T2-Blade acquired in
a transversal orientation. Diffusion weighted imaging was performed in a DTI-sequence
with 3 averages and 20 non-colinear diffusion directions, TR 11500ms, TE 107ms, FOV
2
250mm, voxel size 1.95x1.95x2.2mm, b-value=0 and 1000s/mm in 65 slices.
Data analyses
MR imaging datasets were examined for image quality. The diffusion-weighted volumes
were aligned to their corresponding non-diffusion-weighted (b0) image with an affine
transformation to minimize image distortion from eddy currents and to reduce motion
artifacts. Then, non-brain tissue and background noise were removed from the b0 image
using the Brain Extraction Tool. The diffusion tensor for each voxel was estimated by the
multivariate linear fitting algorithm, and the tensor matrix was diagonalized to obtain its
three pairs of eigenvalues (#1, #2, #3) and eigenvectors. Voxelwise summary parameters
including fractional anisotropy (FA), radial diffusivity (RD) [#= (#2 + #3)/2], axial diffusivity
Page 2 of 12
(AD) [## = #1], and trace [#1 + #2 + #3] were calculated. Group analyses were performed
using tract-based spatial statistics (TBSS) as well as tractography.
A. Tract-Based Spatial Statistics
Whole-brain tract-based spatial statistics (TBSS), a voxel-based standard space group
analysis, was performed. The skeletonized FA, RD, AD, or trace data were used in the
voxel-wise statistics analysis, which is based on a non-parametric approach utilizing
permutation test theory. The testing was performed by the FSL randomise program and
random permutations were set at 5000. Group statistics were carried out on the FA,
RD, AD and trace data. To exclude that any observed difference of diffusion measures
between groups was caused by age-related changes, age was entered into the analysis
as a covariate. For all analyses threshold-free cluster enhancement (TFCE) was used
to obtain the significant differences between two groups at p<0.05, after accounting for
multiple comparisons by controlling for family-wise error (FWE) rate.
B. Tractography
To trace fiber paths of the entire brain, we used the Unscented Kalman filter-based
1, 2
two-tensor tractography algorithm
. Each voxel was randomly seeded 10 times and
each fiber was traced from seed to termination, with the termination criteria of FA<0.15
for the primary tensor component. Subsequently, regions of interest (ROIs) were drawn
individually on the diffusion maps with respect to the color-coded DTI maps using
3DSlicer. Based on the TBSS results the following white matter tracts were chosen:
Corticospinal tract (CST), corpus callosum (CC), and superior longitudinal fasciculus
(SLF). Tractography of the left and right CST was performed by placing an ROI in the
precentral gyrus and another in the ipsilateral, anterior part of the pons. In order to obtain
the callosal tracts, a ROI covering the entire CC was placed in a mid-sagittal slice. The left
3, 4
and right SLF were defined according to the method described by Catani et al. . Once
ROIs were defined, fibers connecting the defined ROIs were extracted. The obtained
tracts were analyzed regarding FA, RD, AD, and trace. We tested for group differences
using the Mann-Whitney U test. A p-value<0.05 (two-sided) was considered statistically
significant. All statistical analyses were performed with SPSS®20.0.0.1.
Results
Conventional MR sequences did not demonstrate visible morphological abnormalities in
either group.
Page 3 of 12
TBSS of 17 soccer players and 16 musicians revealed differences between the two
groups with increased fractional anisotropy (FA) and decreased radial diffusivity (RD)
values in musicians (p<0.05; TFCE-corrected). Compared to soccer players, musicians
demonstrated higher FA values and lower RD values in the right precentral region. This
region contains pathways of the corpus callosum (CC), the right superior longitudinal
fasciculus (SLF), and the right corticospinal tract (CST). The spatial distribution of the
brain region showing increased FA and decreased RD in the musicians is presented in
Figure 1a and b, respectively. Note that there is almost complete overlap between FA
and RD changes. No significant differences were found for AD and trace.
In accordance to the TBSS findings, tractography revealed significantly higher FA and
significantly lower RD values in the right SLF in the musicians when compared to the
soccer players. The right SLF additionally showed a significant decrease in trace values
in musicians. Significantly higher FA and significantly lower RD values were also found
in the left SLF in the musicians group when compared to soccer players. AD values did
not differ significantly between both groups. Figure 2 shows a representative example of
the SLF of both hemispheres, the mean, and p-values as well as the scatter plot in order
to provide a visual depiction of the results and the standard error of the mean.
No significant differences were neither found for the CC nor the CST in either
hemispheres. Figure 3 and 4 show an example of the CSTs and the CC, respectively.
Images for this section:
Page 4 of 12
Fig. 1: FIG. 1. Results of the tract-based spatial statistical analysis (a-b) and respective
scatter plots of subject measures (c-d). Voxels highlighted in red demonstrate significantly
increased FA (a) and decreased RD values (b) in musicians compared to soccer players.
Voxels are thickened into local tracts and displayed on the group mean FA image. Images
are shown according to radiological convention (right = participants' left). Compared with
soccer players, musicians showed higher values for FA (median [IQR] 0.61445 [0.01643]
vs 0.56139 [0.03129], respectively) and decreased values for RD (0.00040 [0.00001] vs
0.00045 [0.00001], respectively).
Page 5 of 12
Fig. 2: FIG. 2. Tractography of the superior longitudinal tract (SLF) of both hemispheres
(a) and respective scatter plots of subject measures (b). Tracts were obtained using the
Unscented Kalman filter-based 2-tensor tractography algorithm to trace fiber paths of the
entire brain 1, 2. Fibers of the SLF were separated according to the method described by
Catani et al. 3, 4. Fig. 2a displays a representative result of the SLF of both hemispheres.
Fig. 2b shows the respective scatter plots of subject measures, the mean and p-values,
as well as the stand error of the mean.
Page 6 of 12
Fig. 3: FIG. 3. Tractography of the callosal tract. Tracts were obtained using the
Unscented Kalman filter-based 2-tensor tractography algorithm to trace fiber paths of the
entire brain 1, 2. Fibers of the CC were separately filtered through a ROI covering the
entire CC in a midsaggital slice. Fig. 3b shows the respective scatter plots of subject
measures, the mean and p-values, as well as the stand error of the mean.
Page 7 of 12
Fig. 4: FIG. 4. Tractography of the corticospinal tract of the left and right hemisphere.
Tracts were obtained using the Unscented Kalman filter-based 2-tensor tractography
algorithm to trace fiber paths of the entire brain 1, 2. Fibers were separately filtered
through the precentral gyrus and the anterior pons for each side.
Page 8 of 12
Conclusion
Advanced DTI methods revealed white matter differences between musicians and soccer
players indicating that long-term motor training leads to different patterns of white matter
organization. Significant results were especially found within the SLF. The SLF connects
parietal and auditory cortex areas and is purported to be a key component of visuospatial
orientation and higher order motor function.
5-7
. High FA, low RD and low trace values are
8, 9
known to be associated with thicker myelin sheaths and axon diameter . The obtained
group differences in white matter integrity may therefore be due to neuroplastic changes
in musicians due to intensive bilateral training of higher order motor skills since childhood
10-12
. Here it has to be mentioned that also contrary results have been published by Imhof
13
et al., showing a training induced increase in diffusivity and decreased FA values . In
the light of current studies on white matter changes in soccer players by Koerte et al our
findings may also be due to repetitive mild traumatic brain injury, i.e. by heading a soccer
ball, within the group of soccer players
the origin of these changes.
8, 14-20
. Further studies are needed to elucidate
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Personal Information
David Kaufmann MD, Institute for Clinical Radiology, University Hospitals Munich,
Ludwig-Maximilians-University Munich, Germany, and Psychiatry Neuroimaging
Laboratory, Brigham and Women´s Hospital, Harvard University, Boston, MA, USA
Inga K Koerte MD, Institute for Clinical Radiology, University Hospitals Munich, LudwigMaximilians-University Munich, Germany, and Psychiatry Neuroimaging Laboratory,
Brigham and Women´s Hospital, Harvard University, Boston, MA, USA
Marc Mühlmann, Institute for Clinical Radiology, University Hospitals Munich, LudwigMaximilians-University Munich, Germany
Elisabeth Hartl MD, formerly Psychiatry Neuroimaging Laboratory, Brigham and Women
´s Hospital, Harvard University, Boston, MA, USA, currently Department of Neurology,
University Hospitals Munich, Ludwig-Maximilians-University Munich, Germany
Maximilian F Reiser MD, Prof. Dr. Dr. h.c. FACR/FRCR, Director of the Institute for
Clinical Radiology, University Hospitals Munich, Ludwig-Maximilians-University Munich,
Germany
Nikos Makris MD/PhD, Associate Professor at Psychiatry Neuroimaging Laboratory,
Brigham and Women´s Hospital, Harvard University, and Associate Director of the Center
for Morphometric Analysis, Department of Neurology at Massachusetts General Hospital,
Boston, MA, USA
Yogesh Rathi PhD, Assistant Professor at Psychiatry Neuroimaging Laboratory, Brigham
and Women´s Hospital, Harvard University, Boston, MA, USA
Martha E Shenton PhD, Professor and Director at Psychiatry Neuroimaging Laboratory,
Brigham and Women's Hospital, Harvard University, Boston, MA, USA
Page 11 of 12
Birgit Ertl-Wagner MD, Prof. Dr., Institute for Clinical Radiology, University Hospitals
Munich, Ludwig-Maximilians-University Munich, Germany
Page 12 of 12