Spatiotemporal neurodynamic mapping of tinnitus from pre-sleep through sleep cycles

Tinnitus manifests as phantom sounds arising from hyperactivity within the auditory pathway, significantly degrading sleep quality. However, the precise mechanisms by which aberrant neural network activation disrupts sleep onset and the extent to which this disruption persists across subsequent sleep stages in tinnitus patients remain largely unknown. In this study, we collected scalp electroencephalogram (EEG) data from 52 tinnitus patients and 52 age- and sex-matched controls throughout the entire sleep process. Based on the hypothesis that cortical hyperarousal is a potential core mechanism underlying sleep disruption in tinnitus, we employed a baseline-correction analysis approach to generate a time- (state-) contingent hyperarousal metric. This aimed to identify abnormal cortical neurodynamics during pre-sleep eyes-closed (EC) relaxation and subsequent sleep stages. The results unveiled a distinctive hierarchical neurodynamic pattern: Patients exhibited typical hyperarousal in the temporal regions during EC relaxation; this hyperarousal redistributed toward the prefrontal cortex across sleep stages and extended to broader parietal-occipital regions during rapid eye movement (REM) sleep. Furthermore, we elucidated the neural correlates underlying clinical behavioral abnormalities related to sleep-onset and maintenance difficulties in tinnitus patients. Additionally, hyperarousal-associated neural patterns in tinnitus patients were consistently validated by two supplementary metrics throughout the sleep cycle. Overall, these findings on neurodynamic spatiotemporal patterns are likely attributable to significant changes in regional activation and inhibition during brain state transitions. These insights not only deepen our understanding of the pathological neural network mechanisms behind sleep-related tinnitus but also offer mechanistic guidance for interventions targeting the wake-sleep continuum in tinnitus management.