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Abstract Modeling the functionality of the human brain is a major goal in neuroscience for which many powerful methodologies have been developed over the last decade. The impact of working memory and the associated brain regions on the brain dynamics is of particular interest due to their connection with many functions and malfunctions in the brain. In this context, the concept of brain flexibility has been developed for the characterization of brain functionality. We discuss emergence of brain flexibility that is commonly measured by the identification of changes in the cluster structure of co-active brain regions. We provide evidence that brain flexibility can be modeled by a system of coupled FitzHugh-Nagumo oscillators where the network structure is obtained from human brain Diffusion Tensor Imaging (DTI). Additionally, we propose a straightforward and computationally efficient alternative macroscopic measure, which is derived from the Pearson distance of functional brain matrices. This metric exhibits similarities to the established patterns of brain template flexibility that have been observed in prior investigations. Furthermore, we explore the significance of the brain’s network structure and the strength of connections between network nodes or brain regions associated with working memory in the observation of patterns in networks flexibility. This work enriches our understanding of the interplay between the structure and function of dynamic brain networks and proposes a modeling strategy to study brain flexibility.