Desync and connect: noninvasive MEG evidence of zero-phase coupling between locally desynchronized regions

Abstract

A prevailing assumption in systems neuroscience is that long-range phase coupling between cortical regions requires locally synchronized oscillatory activity within each interacting area. Here we test whether this assumption holds at the macroscopic level by examining whether distal phase coupling can be detected from MEG data when both interacting regions undergo concurrent event-related desynchronization. Using controlled simulations with progressively disrupted local phase coherence, we first establish that the Context-Dependent PSIICOS (CD-PSIICOS) framework - a projection-based connectivity estimator that separates power-dominated spatial leakage from interaction-specific cross-spectral structure - can recover distal coupling under increasing local phase dispersion. We then apply this framework to empirical MEG recordings from a center-out reaching task in healthy participants. In both the alpha (8-13 Hz) and beta (15-25 Hz) bands, we identify time windows in which robust distal phase coupling emerges between regions exhibiting pronounced movement-related desynchronization. A rank-dependent subpopulation analysis, in which the projection rank is systematically varied to progressively suppress power-related confounds, classifies local networks into leakage-resistant and leakage-driven categories. In the alpha band, no local subpopulation exceeds baseline coupling levels at any projection rank, indicating that interhemispheric coordination operates without detectable local oscillatory support. In the beta band, a more graded pattern is observed: the earliest post-movement window shows above-baseline leakage-resistant local pairs consistent with residual subpopulation-level phase structure, while later windows show reduced decoupling without genuine local synchronization. Phase concentration analysis independently confirms that the detected distal interactions reflect genuine phase-locked coupling in both bands. These results demonstrate that local synchrony is not a necessary prerequisite for long-range phase coupling at the macroscopic level and that this dissociation is accessible to noninvasive MEG when leakage-aware connectivity estimation is employed.