Sensory-guided actions entail the processing of sensory information, generation of perceptual decisions, and the generation of appropriate actions. Neuronal activity underlying these processes is distributed into sensory, fronto-parietal, and motor brain areas, respectively. How the neuronal processing is coordinated across these brain areas to support functions from perception to action remains unknown. We investigated whether phase synchronization in large-scale networks coordinate these processes. We recorded human cortical activity with magnetoencephalography (MEG) during a task in which weak somatosensory stimuli remained unperceived or were perceived. We then assessed dynamic evolution of phase synchronization in large-scale networks from source-reconstructed MEG data by using advanced analysis approaches combined with graph theory. Here we show that perceiving and reporting of weak somatosensory stimuli is correlated with sustained strengthening of large-scale synchrony concurrently in delta/theta (3–7 Hz) and gamma (40–60 Hz) frequency bands. In a data-driven network localization, we found this synchronization to dynamically connect the task-relevant, that is, the fronto-parietal, sensory, and motor systems. The strength and temporal pattern of interareal synchronization were also correlated with the response times. These data thus show that key brain areas underlying perception, decision-making, and actions are transiently connected by large-scale dynamic phase synchronization in the delta/theta and gamma bands. Author Summary We studied the functional role of interareal phase synchronization in the perception-to-action cascade. To this end we recorded human cortical activity with magnetoencephalography (MEG) during a task where weak somatosensory stimuli were perceived or remained unperceived. We identified time-resolved large-scale networks of synchronization by using source-reconstructed MEG data with advanced analysis tools and graph theory. We found that perceiving and reporting of weak somatosensory stimuli was correlated with sustained strengthening of large-scale phase synchronization concurrently in delta/theta (3–7 Hz) and gamma (40–60 Hz) frequency bands. Synchronization characterizing the perceived stimuli connected the sensorimotor system with frontoparietal attentional systems. These data suggest that large-scale network synchronization may coordinate neuronal processing across brain regions during perception, decision-making, and when responding to weak somatosensory stimuli.

Scale-free neuronal dynamics and interareal correlations are emergent characteristics of spontaneous brain activity. How such dynamics and the anatomical patterns of neuronal connectivity are mutually related in brain networks has, however, remained unclear. We addressed this relationship by quantifying the network colocalization of scale-free neuronal activity—both neuronal avalanches and long-range temporal correlations (LRTCs)—and functional connectivity (FC) by means of intracranial and noninvasive human resting-state electrophysiological recordings. We found frequency-specific colocalization of scale-free dynamics and FC so that the interareal couplings of LRTCs and the propagation of neuronal avalanches were most pronounced in the predominant pathways of FC. Several control analyses and the frequency specificity of network colocalization showed that the results were not trivial by-products of either brain dynamics or our analysis approach. Crucially, scale-free neuronal dynamics and connectivity also had colocalized modular structures at multiple levels of network organization, suggesting that modules of FC would be endowed with partially independent dynamic states. These findings thus suggest that FC and scale-free dynamics—hence, putatively, neuronal criticality as well—coemerge in a hierarchically modular structure in which the modules are characterized by dense connectivity, avalanche propagation, and shared dynamic states. Author Summary The framework of criticality has been suggested to explain the scale-free dynamics of neuronal activity in complex interaction networks. However, the in vivo relationship between scale-free dynamics and functional connectivity (FC) has remained unclear. We used human intracranial and noninvasive electrophysiological measurements to map scale-free dynamics and connectivity. We found that the propagation of fast activity avalanches and the interareal coupling of slow, long-range temporal correlations—two key forms of scale-free neuronal dynamics—were nontrivially colocalized with the strongest functional connections. Most importantly, scale-free dynamics and FC exhibited similar modular network structures. FC and scale-free dynamics, and possibly also neuronal criticality, appear to co-emerge in a modular architecture in which the modules are characterized internally by shared dynamic states, avalanche propagation, and dense functional connectivity.