A systematic review and coordinate-based meta-analysis of resting-state fMRI in athletes from open and closed skills sports

Abstract

The impact of prolonged sports training on athletes' brain functional activity remains inconclusive. A systematic review and coordinate-based meta-analysis of resting-state functional magnetic resonance imaging (rs-MRI) is necessary to identify functional connectivity changes induced by prolonged sports training. A total of 31 studies were included in the systematic review, and 18 studies with 347 non-athletes and 327 athletes were analyzed using coordinate-based activation likelihood estimation (ALE) and seed-based d mapping with permutation of subject images (SDM-PSI) meta-analysis. Results revealed that greater functional connectivity in athletes in the paracentral lobule, medial frontal gyrus, precuneus, inferior parietal lobule, supramarginal gyrus, inferior frontal gyrus, Rolandic operculum, and median cingulate/paracingulate gyri (DCG). Consistent changes in the DCG were identified in closed-skill sports athletes. Furthermore, increased regional functional activity was observed in the posterior cingulate gyrus, lingual gyrus and cerebellum. Both meta-analytical methods emphasize altered functional activity within the default mode network (DMN), cerebellar network (CBN), ventral attention network (VAN), visual network (VA), and sensorimotor network (SMN). These findings suggest that long-term sport training optimizes connection strength and efficiency in brain regions associated with visual attention, cognitive and motor control in athletes. Overall, our study reveals shared neural adaptations across different types of athletes, offering new insights into the effects of long-term specific training on brain functional connectivity in specialists.

Keywords: Activation likelihood estimation; Athletes; Functional connectivity; Meta-analysis; Resting-state functional magnetic resonance imaging; Seed-based d mapping.

Fig. 1

PRISMA flowchart of study selection. Abbreviations: FC: functional connectivity.

Fig. 2

Methodological characteristics and sports program characteristics of the included studies. (A) A total of 21 seed-based FC (15 included in the meta-analysis) and 29 other non seed-based FC metrics (10 ALFF/fALFF/ReHo included in the meta-analysis) in the systematic review. (B) A total of 14 studies on closed-skill sports and 17 studies on open-skill sports were examined. Table tennis (n = 6), along with endurance running (n = 4) are the most researched. Abbreviations: ALFF: amplitude of low-frequency fluctuation; CGCA: conditional granger causality analysis; DC: degree centrality; fALFF: fractional amplitude of low-frequency fluctuation; FC: functional connectivity; FCD: functional connectivity density; FS: functional stability; ICA: independent component analysis; PreAL: percentage amplitude of fluctuation; ReHo: regional homogeneity; ROI: regions of interest; VMHC: voxel-mirrored homotopic connectivity.

Fig. 3

Results of altered resting-state functional activity in different types of athletes based on activation likelihood estimation meta-analysis. Compared with health controls, athletes showed (A) enhanced FC in PCL, MeFG, precuneus and IPL; (B) enhanced ALFF, fALFF, ReHo in right PCG and LG. Abbreviations: ALFF: amplitude of low-frequency fluctuation; fALFF: fractional ALFF; FC: functional connectivity; IPL: inferior parietal lobule; LG: lingual gyrus; MeFG: medial frontal gyrus; PCG: posterior cingulate gyrus; PCL: paracentral lobule; ReHo: regional homogeneity.

Fig. 4

Results of altered resting-state functional activity in different types of athletes based on seed-based d mapping with permutation of subject Images meta-analysis. Compared with health controls, athletes showed (A) enhanced FC in DCG, SMG, RO and IFG; (B) enhanced FC in DCG in closed-skill sports athletes; (C) enhanced ALFF, fALFF, ReHo in CB. Abbreviations: ALFF: amplitude of low-frequency fluctuation; CB: cerebellum; DCG: median cingulate / paracingulate gyri; fALFF: fractional ALFF; FC: functional connectivity; IFG: inferior frontal gyrus; ReHo: regional homogeneity; RO: rolandic operculum; SMG:supramarginal gyrus.