A multiplex of connectome trajectories enables several connectivity patterns in parallel

Abstract

The large-scale organization of functional connectivity (FC) – the functional connectome – traverses distinct spatial patterns in a dynamic trajectory as demonstrated independently in fMRI and electrophysiological studies. These patterns are thought to satisfy ever-changing processing demands. FMRI and electrophysiology capture partly non-overlapping neural populations at different timescales, and it remains unknown to what degree the dynamic connectome trajectories across the two modalities are associated. We sought to clarify this relationship by studying resting wakefulness in a rare concurrent intracranial EEG and functional MRI dataset (iEEG-fMRI; 9 human neurosurgical patients) and in whole-brain connectomes obtained from source-localized EEG-fMRI (26 healthy humans). We measured ″spatial convergence″ as cross-modal spatial similarity of connectome configurations at a given time, and ″temporal convergence″ as synchronous occurrence of spatial convergence. We investigated three possible scenarios characterizing the cross-modal association of connectome trajectories: I) spatially and temporally convergent, II) spatially convergent but temporally divergent, and III) spatially and temporally divergent. We found that the behavior of fMRI and iEEG/EEG is consistent with scenario II: connectome trajectories spatially converge at intermittent times. Importantly, such asynchronous spatial convergence of connectome configurations was driven by cross-modally matched recurrent connectome states, independently across electrophysiological timescales. This connectome-level multi-frequency spatial convergence and temporal divergence suggests that hemodynamic and electrophysiological signals capture distinct aspects of FC, rather than serving as intermodal measurements of the same phenomenon. The multitude of flexible trajectories across timescales may concurrently enable FC across multiple independent sets of distributed brain regions.