Network Mechanisms Underlying the Regional Diversity of Variance and Time Scales of the Brain’s Spontaneous Activity Fluctuations

Abstract

The brain’s activity fluctuations have different temporal scales across the brain regions, with associative regions displaying slower timescales than sensory areas. This hierarchy of timescales has been shown to correlate with both structural brain connectivity and intrinsic regional properties. Here, using publicly available human resting-state fMRI and dMRI data, it was found that, while more structurally connected brain regions presented activity fluctuations with longer timescales, their activity fluctuations presented lower variance. The opposite relationships between the structural connectivity and the variance and temporal scales of resting-state fluctuations, respectively, were not trivially explained by simple network propagation principles. To understand these structure–function relationships, two commonly used whole-brain models were studied, namely, the Hopf and Wilson–Cowan models. These models use the brain’s connectome to couple local nodes (representing brain regions) displaying noise-driven oscillations. The models show that the variance and temporal scales of activity fluctuations can oppositely relate to connectivity within specific parameter regions, even when all nodes have the same intrinsic dynamics—but also when intrinsic dynamics are constrained by the myelinization-related macroscopic gradient. These results show that, setting aside intrinsic regional differences, connectivity and network state are sufficient to explain the regional differences in fluctuations’ scales. State dependence supports the vision that structure–function relationships can serve as biomarkers of altered brain states. Finally, the results indicate that the hierarchies of timescales and variances reflect a balance between stability and responsivity, with greater and faster responsiveness at the network periphery, while the network core ensures overall system robustness.