Pairwise Interactions among Brain Regions Organize Large-Scale Functional Connectivity during Execution of Various Tasks

• Published in: Neuroscience Vol. 412; pp. 190 - 206
• Main Authors: Niu, Weikun, Huang, Xuhui, Xu, Kaibin, Jiang, Tianzi, Yu, Shan
• Format: Journal Article
• Language: English
• Published: United States Elsevier Ltd 01.08.2019
• Subjects: Brain - diagnostic imaging; Brain Mapping; Cognition - physiology; Emotions - physiology; functional network; Humans; Magnetic Resonance Imaging; Nerve Net - diagnostic imaging; neural network model; Neural Networks, Computer; pairwise correlation; Psychomotor Performance - physiology; task state fMRI; task state fMRI; neural network model; pairwise correlation; functional network
• ISSN: 0306-4522; 1873-7544; 1873-7544
• DOI: 10.1016/j.neuroscience.2019.05.011

Spatially separated brain areas interact with each other to form networks with coordinated activities, supporting various brain functions. Interaction structures among brain areas have been widely investigated through pairwise measures. However, interactions among multiple (e.g., triple and quadruple) areas cannot be reduced to pairwise interactions. Such higher order interactions (HOIs), e.g., exclusive-or (XOR) operation, are widely implemented in computation systems and are crucial for effective information processing. However, it is currently unclear whether any HOIs are present in large-scale brain functional networks when subjects are executing specific tasks. Here we analyzed functional magnetic resonance imaging (fMRI) data collected from human subjects executing various perceptual, motor, and cognitive tasks. We found that HOI strength in the macroscopic functional networks was very weak for all tasks, suggesting that major brain activities do not rely on HOIs on the macroscopic level at the timescale of hundreds of milliseconds. These weak HOIs during tasks were further investigated with a neural network model activated by external inputs, which suggested that weak pairwise interactions among brain areas organized the system without involving HOIs. Taken together, these results demonstrated the dominance of pairwise interactions in organizing coordinated activities among different brain areas to support various brain functions. •The lack of HOIs at functional brain networks was revealed during various tasks.•The weakly coupled regime of macroscopic brain networks was suggested.•The lack of HOIs provides the methodological foundation for pairwise approaches.