The optimal organization for functional segregation and integration in brain is made evident by the “small-world” feature of functional connectivity (FC) networks and is further supported by the loss of this feature that has been described in many types of brain disease. However, it remains unknown how such optimally organized FC networks arise from the brain’s structural constrains. On the other hand, an emerging literature suggests that brain function may be supported by critical neural dynamics, which is believed to facilitate information processing in brain. Though previous investigations have shown that the critical dynamics plays an important role in understanding the relation between whole brain structural connectivity and functional connectivity, it is not clear if the critical dynamics could be responsible for the optimal FC network configuration in human brains. Here, we show that the long-range temporal correlations (LRTCs) in the resting state fMRI blood-oxygen-level-dependent (BOLD) signals are significantly correlated with the topological matrices of the FC brain network. Using structure-dynamics-function modeling approach that incorporates diffusion tensor imaging (DTI) data and simple cellular automata dynamics, we showed that the critical dynamics could optimize the whole brain FC network organization by, e.g., maximizing the clustering coefficient while minimizing the characteristic path length. We also demonstrated with a more detailed excitation-inhibition neuronal network model that loss of local excitation-inhibition (E/I) balance causes failure of critical dynamics, therefore disrupting the optimal FC network organization. The results highlighted the crucial role of the critical dynamics in forming an optimal organization of FC networks in the brain and have potential application to the understanding and modeling of abnormal FC configurations in neuropsychiatric disorders.

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