This study employed both VBM and SBM to investigate gray matter characteristics in the soccer population. The results revealed significant increases in the volume of the cerebellum, thalamus, and calcarine cortex. Then, we further constructed a CaSCN to explore the temporal priority relationship among these gray matter increasing regions.
This study is the first to utilize both univariate and multivariate approaches to investigate the impact of soccer training on gray matter morphological changes. Both approaches consistently revealed a significantly larger gray matter volume in the cerebellum of the soccer group compared to the control group. SBM demonstrated greater sensitivity, enabling a more comprehensive detection of gray matter morphological changes, while VBM exhibited higher specificity in facilitating the exploration of the most prominent brain regions with deformation. Thus, combining these two methods provides a more comprehensive understanding of the relationship between gray matter morphological changes and soccer training.
In line with the research hypothesis, the most significant gray matter morphological changes were observed in the cerebellum. Specifically, significant differences were observed in left cerebellum_8, right cerebellum_Crus1 and bilateral cerebellum_Crus2/4/5. Additionally, correlation analysis indicated a significant positive correlation between cerebellar volume and years of training. Numerous studies consistently demonstrate that expert athletes in various sports have significantly larger cerebellar gray matter volume compared to non-athletes28–31. Animal studies also showed that glial volume Purkinje cell, volume of the molecular layer, number of synapses, and dendrite size of stellate cells in the cerebellum were significantly larger in acrobat-trained rats compared to rats engaged in a sedentary lifestyle32–34. These findings suggest that physical training can significantly modify the structural plasticity of the cerebellum. The left cerebellum_8 and bilateral cerebellum_4/5 are essential components of the cerebellar motor module, playing a crucial role in controlling motor-related functions such as balance, posture, and motor learning35. These brain regions are of particular significance in the context of soccer, as they serve as the foundation for players to execute complex technical movements with precision and skill. Soccer requires saccadic eye movements for tracking and intercepting the ball in motion. Recent fMRI studies have shown that the cerebellum_Crus6/7 regions are activated during visually guided rapid eye movements36. Additionally, the right cerebellum_Crus1 and bilateral cerebellum_Crus2 are part of the cerebellar cognitive modules and closely linked to executive functions and semantic process. Beyond the motor module of the cerebellum, which primarily responds to sensorimotor information, the ability to comprehend the intention of an action, and even the underlying strategy at a more abstract level, likely depends on the cerebellum’s cognitive module. Hence, we hypothesized that an increase in gray matter in the cerebellum_Crus1/2 could be associated with improved sports decision-making or prediction resulting from long-term soccer training.
SBM results also demonstrated larger gray matter volume in the bilateral thalamus and Calcarine regions, indicating to some extent that SBM is more sensitive in detecting gray matter morphological changes compared to VBM. The thalamus plays a crucial role in the brain, receiving neural projections from the cortex, cerebellum, and subcortex37. It acts as a key node in both the direct and indirect pathways, facilitating the integration of information from the basal ganglia and transmitting it to the supplementary motor area, leading to the inhibition or activation of corresponding actions38. Thus, the thalamus serves as a central relay station in the brain. Previous studies have found that soccer experts exhibit superior response inhibition ability, which is significantly related to thalamic gray matter volume20. Therefore, the increasing thalamic gray matter volume may indicate more coordinated functioning of various action control circuit, facilitating the execution of soccer techniques and tactics.
The calcarine region, located in the posterior part of the occipital lobe, plays a crucial role in visual spatial processing39. Previous resting-state brain imaging studies have found that soccer experts exhibit significantly greater recruitment capacity in the visual network compared to novices. Studies have indicated that the calcarine region is part of the action observation network (AON), playing a vital role in action learning and prediction processes 40,41. However, in terms of structural research, there have been few studies demonstrating a significant increase in calcarine gray matter volume among skilled athletes. This phenomenon can be attributed, on one hand, to the constraints of univariate research methods, and on the other hand, to the fact that previous studies have mostly focused on closed-skill sports such as long-distance running, diving, or gymnastics, where athletes do not heavily rely on visual information to adjust their movements. In contrast, soccer, as a complex team sport, takes place in large and populated competition fields, and vision serves as the primary source of information for players to make sporting decisions and predictions. Thus, visual spatial functionality plays a crucial role in the athlete's process of filtering movement information during gameplay. Research has indicated significant differences in the visual gaze patterns between soccer experts and novices. Compared to novices, soccer experts demonstrate higher gaze efficiency, characterized by rapid rejection of distractions, prolonged fixation on critical areas, and a broader gaze scope, allowing them to gather global information effectively. Furthermore, a comprehensive review of studies suggests that during predictive tasks, the visual cortex activation is stronger in skilled athletes. Therefore, the observed increase in calcarine volume may indicate a potential neural basis for the efficient gaze patterns exhibited by soccer players. However, these findings require further validation.
Changes in brain structure over time are best evaluated in longitudinal studies. However, results from this work suggest the potential for assessing temporal changes in the structure of the brain by applying granger causality analysis to morphometric data classified according to training duration. The CaSCN revealed that structural changes in one region precede and allow prediction of the change in another region in relationship to the training peroid42. The results of CaSCN demonstrated that the thalamus served as the central hub of the GCA network, with thalamic changes potentially causally linked to all other nodes. During the initial phases of soccer training, interregional information transmission among different brain regions is not yet coordinated. As a relay station in the brain, an increase in thalamic volume has the potential to promote information integration across brain regions and facilitate the rapid acquisition of motor skills43,44. Consequently, changes in thalamic gray matter volume may manifest earlier than in other brain regions. There are significant positive GC connections between the cerebellum and the calcarine, suggesting that an increase in calcarine gray matter volume occurs prior to cerebellar changes. Soccer involves complex visual information processing, requiring players to quickly perceive and analyze the movement of the ball, teammates, and opponents on the field45. This heightened visual demand may lead to early structural adaptations in the primary visual cortex to enhance visual acuity and processing capabilities. As soccer training progresses, players continuously refine their motor skills and coordination, which heavily rely on the cerebellum's functions. The cerebellum plays a crucial role in motor learning and coordination, making it susceptible to adaptations as soccer players develop and refine their skills over time. Longitudinal studies have also indicated that during the process of juggle training, there is an earlier increase in gray matter volume in the visual cortex compared to the motor control regions46,47.
This study utilized VBM and SBM methods to depict brain structural characteristics in individuals with regular soccer training. A combination of univariate and multivariate methods was employed to provide comprehensive information. The findings confirmed that soccer training significantly increased gray matter volume in the cerebellum, thalamus, and calcarine. Moreover, the thalamus may play a central role in driving the augmentation of gray matter in other brain regions.