Enhanced structural connectivity within the motor loop in professional boxers prior to a match

Abstract

Professional boxers train to reduce their body mass before a match to refine their body movements. To test the hypothesis that the well-defined movements of boxers are represented within the motor loop (cortico-striatal circuit), we first elucidated the brain structure and functional connectivity specific to boxers and then investigated plasticity in relation to boxing matches. We recruited 21 male boxers 1 month before a match (Time1) and compared them to 22 age-, sex-, and body mass index (BMI)-matched controls. Boxers were longitudinally followed up within 1 week prior to the match (Time2) and 1 month after the match (Time3). The BMIs of boxers significantly decreased at Time2 compared with those at Time1 and Time3. Compared to controls, boxers presented significantly higher gray matter volume in the left putamen, a critical region representing motor skill training. Boxers presented significantly higher functional connectivity than controls between the left primary motor cortex (M1) and left putamen, which is an essential region for establishing well-defined movements. Boxers also showed significantly higher structural connectivity in the same region within the motor loop from Time1 to Time2 than during other periods, which may represent the refined movements of their body induced by training for the match.

Figure 1

General design. We included 21 licensed male boxers and 22 age-, sex-, and BMI-matched controls. We followed up boxers at time points Time2 and Time3. All imaging statistical thresholds for VBM and rs-fMRI were set to uncorrected p < 0.001 at the voxel level, and FWE-corrected p < 0.05, at the cluster level. FWE, family-wise error; rs-fMRI, resting-state functional magnetic resonance imaging; VBM, voxel-based morphometry.

Figure 2

Body mass index of controls and boxers. The boxer BMI at Time2 was significantly decreased [F(2, 59) = 10.21, p < 0.01] in repeated measures ANOVA. Bonferroni correction was used for the post-hoc analysis. BMI, body mass index; n.s., not significant.

Figure 3

Boxers’ specific structural anatomy ([Boxers (Time1) > Controls]). The location of a significantly larger cluster in the left OFC and left putamen of boxers are shown as red and blue regions, respectively, on the z-axis. The statistical threshold for significant differences was set to FWE-corrected p < 0.05, at the cluster level, with uncorrected p < 0.001 at the voxel level. Lt, left; OFC, orbitofrontal cortex.

Figure 4

Boxers’ specific functional connectivity ([Boxers (Time1) > Controls]). (a) The statistical contrast between boxers and controls when seeding the left OFC (shown in red) delineated significant functional connectivity with the left hippocampus and the right MTG (shown in yellow colour respectively). (b) The statistical contrast between boxers and controls when seeding the left putamen (shown in blue) delineated significant functional connectivity with the left M1 cluster including the left premotor and anterior insular cortex, the left postCG, and Rt. IFG cluster including the right anterior insular cortex (shown in cyan colour respectively). The statistical threshold for significance was set at FWE-corrected p < 0.05 at the cluster level, with an uncorrected p < 0.001 at the voxel level. Lt, left; Rt, right; M1, primary motor cortex; MTG, middle temporal gyrus; postCG, postcentral gyrus; IFG, inferior frontal gyrus.

Figure 5

The functional connectivity area correlated with BMI decrease in Time2. The functional connectivity area (shown in red) that correlated with a decrease in BMI, seeding the left putamen cluster (shown in blue) at Time2, is shown. The M1 cluster is indicated by a red arrow. Using the eigenvariate function in SPM, we extracted the average beta value (as the functional connectivity value) in the sphere of an 8-mm radius (16-mm diameter) located at the peak of the left M1 cluster, based on our hypothesis testing the representation within the motor loop of boxers. The right scatter graph indicates a significant correlation (R² = 0.3076, [p = 0.011]) between the decrease in BMI and the average beta value within the sphere of the left M1 cluster at Time2. BMI, body mass index; M1, primary motor cortex; SPM, statistical parametric mapping.

Figure 6

Diffusion tractography and the number of streamlines from the Lt. putamen to Lt. M1. (a) Seed and target brain regions used in diffusion tractography analysis are shown in red; These region-of-interests were defined based on the results from group-level analyses in the resting-state functional connectivity: from Lt. OFC (seed) to Lt. hippocampus and right MTG, and from Putamen (seed) to Lt. M1, Lt. postcentral gyrus and right IFG. b) Representative images of tractography results from the Lt. Putamen to Lt. M1 for a subject, are illustrated. Streamlines were originally drawn in native space, and then were transformed into MNI space. (c) The number of streamlines from the Lt. putamen to Lt. M1 in controls and boxers (Time1, Time2, and Time3). Only the number of streamlines from Lt. putamen to Lt. M1 between Time1 and Time2 in boxers shows a significant increase [F(2, 40) = 4.76, p = 0.02] in repeated measures ANOVA. Bonferroni correction was used in post-hoc analysis. Lt, left; OFC, orbitofrontal cortex; M1, primary motor cortex; MTG, middle temporal gyrus; IFG, inferior frontal gyrus; ANOVA, analysis of variance.