Neural oscillation mechanisms of repetitive subconcussive impacts: a network study of microstate-specific cross-frequency coupling.

Background: Repetitive subconcussive impacts are linked to headache pathophysiology, yet the role of electroencephalography (EEG) microstates and cross-frequency coupling in repetitive subconcussive (SC) neural alterations remains unclear. This study investigated microstate-specific cross-frequency coupling network (MCFCN) abnormalities in SC-exposed individuals to uncover mechanisms underlying headache vulnerability.

Methods: Resting-state EEG was recorded from 16 experienced male parachuters aged 18-25 years (SC group) and 16 demographically matched healthy male controls of the same age range (HC group). Microstate analysis (four canonical classes: A-D) and cross-frequency coupling (CFC) interactions (n: m) phase synchronization index, PSI) were computed to construct the MCFCNs. The MCFCNs were evaluated using machine learning (LightGBM classifier) to discriminate between the two groups, with key features identified by SHAP values and corrected for multiple comparisons.

Results: SC-exposed individuals exhibited MCFCN disruptions in large-scale networks. Notably, reduced delta/theta to alpha/beta coupling was observed in microstates A, C, and D, except for an increase in delta-band coupling from the default mode network (DMN) to the frontoparietal network (FPN) in microstate A. These alterations involved emotional-motor integration, attentional control, and self-referential processing. LightGBM models achieved significant group discrimination, with SHAP analysis highlighting theta-DMN, beta-SMN, and delta-LIM as critical nodes.

Conclusions: SC exposure induces MCFCNs abnormalities resembling central pain syndromes, even in the absence of overt symptoms. These findings suggest that interactions within MCFCNs may serve as potential early biomarkers for headache vulnerability and chronicity, warranting further exploration in longitudinal studies and targeted neurointerventions.