Dynamic reconfiguration of frontal brain networks during executive cognition in humans

Significance Cognitive flexibility is hypothesized to require dynamic integration between brain areas. However, the time-dependent nature and distributed complexity of this integration remains poorly understood. Using recent advances in network science, we examine the functional integration between brain areas during a quintessential task that requires executive function. By linking brain regions (nodes) by their interactions (time-dependent edges), we uncover nontrivial modular structure: groups of brain regions cluster together into densely interconnected structures whose interactions change during task execution. Individuals with greater network reconfiguration in frontal cortices show enhanced memory performance, and score higher on neuropsychological tests challenging cognitive flexibility, suggesting that dynamic network reconfiguration forms a fundamental neurophysiological mechanism for executive function. The brain is an inherently dynamic system, and executive cognition requires dynamically reconfiguring, highly evolving networks of brain regions that interact in complex and transient communication patterns. However, a precise characterization of these reconfiguration processes during cognitive function in humans remains elusive. Here, we use a series of techniques developed in the field of “dynamic network neuroscience” to investigate the dynamics of functional brain networks in 344 healthy subjects during a working-memory challenge (the “n-back” task). In contrast to a control condition, in which dynamic changes in cortical networks were spread evenly across systems, the effortful working-memory condition was characterized by a reconfiguration of frontoparietal and frontotemporal networks. This reconfiguration, which characterizes “network flexibility,” employs transient and heterogeneous connectivity between frontal systems, which we refer to as “integration.” Frontal integration predicted neuropsychological measures requiring working memory and executive cognition, suggesting that dynamic network reconfiguration between frontal systems supports those functions. Our results characterize dynamic reconfiguration of large-scale distributed neural circuits during executive cognition in humans and have implications for understanding impaired cognitive function in disorders affecting connectivity, such as schizophrenia or dementia.