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Reconfiguration of brain network dynamics by paresthesia-based spinal cord stimulation in herpes zoster-associated
Ying Yang1, Li Chen2, Haocheng Zhou3
1Hunan Key Laboratory of Nanophotonics and Devices, Hunan Key Laboratory of Super-Microstructure and Ultrafast Process, School of Physics, Central South University, Changsha, China; Department of Pain, The Third Xiangya Hospital and Institute of Pain Medicine, Central South University, Changsha, China.
Background:
Neuropathic pain is characterized by disrupted large-scale brain dynamics. While paresthesia-based spinal cord stimulation (SCS) offers superior efficacy compared to pharmacological interventions, its clinical potential is constrained by poorly understood central mechanisms. EEG microstate analysis provides a powerful framework for capturing rapid spatiotemporal brain dynamics, offering further insights to elucidate how SCS potentially reconfigures the organization of neural activity.
Methods:
We recruited patients with acute and chronic herpes zoster-associated neuralgia (HZAN) to investigate the modulatory effects of SCS. Using a Group (acute vs. chronic) × Condition (SCS-on vs. SCS-off) interaction design, we evaluated topographies, temporal metrics, and microstate-based functional connectivity to comprehensively characterize condition-dependent brain dynamics.
Results:
SCS significantly attenuated the temporal predominance (duration, coverage, and occurrence) of Microstate A (auditory/visual and arousal), accompanied by a reciprocal expansion of Microstate B (visual network). Transition dynamics were markedly reconfigured, specifically through increased transition probability from A to B and a decrease from C (salience) to A. Intriguingly, exploratory analysis indicated that the transition probability from A to B (SCS-off) was positively correlated with post-treatment VAS scores. Furthermore, microstate-based connectivity analysis captured four functional modulation trends: functional inflexibility, reversal, alignment, and shared modulation. Finally, frequency-specific Microstate-A subnetwork strength emerged as a robust predictor of SCS therapeutic efficacy, particularly in acute HZAN.
Conclusions:
Paresthesia-based SCS potentially functions as a systemic reconfigurator of large-scale brain dynamics. By modulating and reconfiguring the aberrant spatiotemporal architecture and connectivity, SCS holds the potential to nudge the brain away from pathological entrapment toward a more adaptive and flexible functional mode. These results underscore the potential of microstate-based metrics as non-invasive biomarkers for optimizing individualized neuromodulation in HZAN.
