Surrogate data analyses of the energy landscape analysis of resting-state brain activity

The spatiotemporal dynamics of resting-state brain activity can be characterized by switching between multiple brain states, and numerous techniques have been developed to extract such dynamic features from resting-state functional magnetic resonance imaging (fMRI) data. However, many of these techniques are based on momentary temporal correlation and co-activation patterns and merely reflect linear features of the data, suggesting that the dynamic features, such as state-switching, extracted by these techniques may be misinterpreted. To examine whether such misinterpretations occur when using techniques that are not based on momentary temporal correlation or co-activation patterns, we addressed Energy Landscape Analysis (ELA) based on pairwise-maximum entropy model (PMEM), a statistical physics-inspired method that was designed to extract multiple brain states and dynamics of resting-state fMRI data. We found that the shape of the energy landscape and the first-order transition probability derived from ELA were similar between real data and surrogate data suggesting that these features were largely accounted for by stationary and linear properties of the real data without requiring state-switching among locally stable states. To confirm that surrogate data were distinct from the real data, we replicated a previous finding that some topological properties of resting-state fMRI data differed between the real and surrogate data. Overall, we found that linear models largely reproduced the first order ELA-derived features (i.e., energy landscape and transition probability) with some notable differences.