The brains of elite soccer players are subject to experience-dependent alterations in white matter connectivity

Soccer is the only major sport with voluntary unprotected head-to-ball contact. It is crucial to determine if head impact through regular soccer sports training is manifested in brain structure and connectivity, and whether such alterations are due to sustained training per se. Using diffusion tensor imaging, we documented a comprehensive view of soccer players’ brains in a sample of twenty-five right-handed male elite soccer players aged from 18 to 22 years and twenty-five non-athletic controls aged 19 to 24 years. Importantly, none had recalled a history of concussion. We performed a whole-brain tract-based spatial statistical analysis, and a tract-specific probabilistic tractography method to measure differences of white matter properties between groups. Whole-brain integrity analysis showed increased microstructural integrity within the corpus callosum tract in soccer players compared to controls. Further, tract-specific probabilistic tractography revealed that the anterior part of corpus callosum may be the brain structure most relevant to training experience, which may put into perspective prior evidence showing corpus callosum alteration in retired or concussed athletes practicing contact sports. Intriguingly, experience-related alterations showed left hemispheric lateralization of potential early signs of concussion-like effects. This is the first study to-date providing a definitive characterization of soccer-specific experience-related structural alterations. In sum, we concluded that the observed gains and losses may be due to a consequence of engagement in protracted soccer training that incurs prognostic hallmarks associated with minor injury-induced neural inflammation. Soccer is the only major sport with voluntary unprotected head-to-ball contact. It is crucial to determine if head impact through regular soccer sports training is manifested in brain structure and connectivity, and whether such alterations are due to sustained training per se. Using diffusion tensor imaging, we documented a comprehensive view of soccer players’ brains in a sample of twenty-five right-handed male elite soccer players aged from 18 to 22 years and twenty-five non-athletic controls aged 19 to 24 years. Importantly, none had recalled a history of concussion. We performed a whole-brain tract-based spatial statistical analysis, and a tract-specific probabilistic tractography method to measure differences of white matter properties between groups. Whole-brain integrity analysis showed increased microstructural integrity within the corpus callosum tract in soccer players compared to controls. Further, tract-specific probabilistic tractography revealed that the anterior part of corpus callosum may be the brain structure most relevant to training experience, which may put into perspective prior evidence showing corpus callosum alteration in retired or concussed athletes practicing contact sports. Intriguingly, experience-related alterations showed left hemispheric lateralization of potential early signs of concussion-like effects. This is the first study to-date providing a definitive characterization of soccer-specific experience-related structural alterations. In sum, we concluded that the observed gains and losses may be due to a consequence of engagement in protracted soccer training that incurs prognostic hallmarks associated with minor injury-induced neural inflammation. Soccer is the only major sport with voluntary unprotected head-to-ball contact. It is crucial to determine if head impact through regular soccer sports training is manifested in brain structure and connectivity, and whether such alterations are due to sustained training per se. Using diffusion tensor imaging, we documented a comprehensive view of soccer players’ brains in a sample of twenty-five right-handed male elite soccer players aged from 18 to 22 years and twenty-five non-athletic controls aged 19 to 24 years. Importantly, none had recalled a history of concussion. We performed a whole-brain tract-based spatial statistical analysis, and a tract-specific probabilistic tractography method to measure differences of white matter properties between groups. Whole-brain integrity analysis showed increased microstructural integrity within the corpus callosum tract in soccer players compared to controls. Further, tract-specific probabilistic tractography revealed that the anterior part of corpus callosum may be the brain structure most relevant to training experience, which may put into perspective prior evidence showing corpus callosum alteration in retired or concussed athletes practicing contact sports. Intriguingly, experience-related alterations showed left hemispheric lateralization of potential early signs of concussion-like effects. This is the first study to-date providing a definitive characterization of soccer-specific experience-related structural alterations. In sum, we concluded that the observed gains and losses may be due to a consequence of engagement in protracted soccer training that incurs prognostic hallmarks associated with minor injury-induced neural inflammation.

Methods
MRI images were collected on a GE MR750 3T scanner (GE Healthcare, Waukesha, WI, USA) in the Mind Research and Imaging Center of NCKU with a 32-channel brain array coil. All participants were scanned using the same MR scanner. Diffusion-weighted spin-echo echo-planar imaging sequence images were obtained with a measured spatial resolution of 2.5 x 2.5 x 2.5 mm (acquisition matrix 100 x 100 pixels, 50 slices) and a reconstructed resolution of 1.56 x 1.56 x 2.0 mm (reconstructed matrix 100 x 100 pixels, 50 slices). The sequence parameters were repetition time (TR) = 5500ms, echo time (TE) = 62~64 ms, 50 non-linear diffusion directions with b = 1000s/mm2, field of view (FOV) = 250×250 mm2, number of excitations (NEX) = 3, and slice thickness = 2.5 mm. Reverse DTI was also acquired for top-up correction in the DTI preprocessing. The acquisition parameters for the reverse DTI were identical to the DTI except for that only six directions were obtained due to the time constraints. The total acquisition time was 15 minutes 24 seconds.

Three-dimensional high-resolution brain structural images were also acquired using a T1-weighted fast spoiled gradient-echo dual-echo (FSPGR) sequence for each participant to allow for spatial normalization and visualization. The sequence parameters were TR = 2900 ms; TE = 7.6 ms; matrix size 224 x 224; flip angle = 12°; 1 mm slice thickness; FOV = 22.4/1 (cm/Phase); receiver bandwidth (BW) = ±31.25 kHz, and 170 sagittal slices covering the whole brain were collected. The total acquisition time was 3 minutes 38 seconds. For each participant, all the diffusion and anatomical images were acquired in the same session.