Topology of Functional Connectivity and Hub Dynamics in the Beta Band As Temporal Prior for Natural Vision in the Human Brain

Networks hubs represent points of convergence for the integration of information across many different nodes and systems. Although a great deal is known on the topology of hub regions in the human brain, little is known about their temporal dynamics. Here, we examine the static and dynamic centrality of hub regions when measured in the absence of a task (rest) or during the observation of natural or synthetic visual stimuli. We used Magnetoencephalography (MEG) in humans (both sexes) to measure static and transient regional and network-level interaction in α- and β-band limited power (BLP) in three conditions: visual fixation (rest), viewing of movie clips (natural vision), and time-scrambled versions of the same clips (scrambled vision). Compared with rest, we observed in both movie conditions a robust decrement of α-BLP connectivity. Moreover, both movie conditions caused a significant reorganization of connections in the α band, especially between networks. In contrast, β-BLP connectivity was remarkably similar between rest and natural vision. Not only the topology did not change, but the joint dynamics of hubs in a core network during natural vision was predicted by similar fluctuations in the resting state. We interpret these findings by suggesting that slow-varying fluctuations of integration occurring in higher-order regions in the β band may be a mechanism to anticipate and predict slow-varying temporal patterns of the visual environment. SIGNIFICANCE STATEMENT A fundamental question in neuroscience concerns the function of spontaneous brain connectivity. Here, we tested the hypothesis that topology of intrinsic brain connectivity and its dynamics might predict those observed during natural vision. Using MEG, we tracked the static and time-varying brain functional connectivity when observers were either fixating or watching different movie clips. The spatial distribution of connections and the dynamics of centrality of a set of regions were similar during rest and movie in the β band, but not in the α band. These results support the hypothesis that the intrinsic β-rhythm integration occurs with a similar temporal structure during natural vision, possibly providing advanced information about incoming stimuli.