The influence of nonlinear resonance on human cortical oscillations

Abstract Whether macroscale brain signals reflect linear or nonlinear organization remains poorly characterized. This distinction matters for modeling neural dynamics and interpreting oscillatory biomarkers of cognition and disease. Spectral analysis reveals aperiodic broadband and rhythmic narrowband components but does not capture nonlinear resonance, such as quadratic phase coupling among oscillations, which requires higher-order spectral analysis. We introduce BiSpectral EEG Component Analysis (BiSCA), combining spectral and bispectral analysis to separate aperiodic (Xi) from rhythmic (Rho) components, localize nonlinear signatures, and distinguish nonlinearity from non-Gaussianity; simulations confirm this separation. Applying BiSCA to two large datasets (1771 intracranial channels; 960 scalp EEG subjects), we detect significant nonlinear or non-Gaussian structure in 81.6% of scalp EEG and 67.9% of iEEG channels; forward modeling indicates the higher scalp prevalence reflects volume-conduction spread of focal nonlinear sources. In spatially focal iEEG, aperiodic Xi shows no detectable quadratic nonlinearity or non-Gaussianity, whereas Rho components, including Alpha and Mu, carry the dominant cortical quadratic coupling. Despite higher occipital Alpha power, the strongest nonlinear signatures arise from parietal Mu. Nonlinear resonance is thus expressed primarily through oscillatory rather than aperiodic dynamics.