The Control of Global Brain Dynamics: Opposing Actions of Frontoparietal Control and Default Mode Networks on Attention

Abstract

Understanding how dynamic changes in brain activity control behavior is a major challenge of cognitive neuroscience. Here, we consider the brain as a complex dynamic system and define two measures of brain dynamics: the synchrony of brain activity, measured by the spatial coherence of the BOLD signal across regions of the brain; and metastability, which we define as the extent to which synchrony varies over time. We investigate the relationship among brain network activity, metastability, and cognitive state in humans, testing the hypothesis that global metastability is "tuned" by network interactions. We study the following two conditions: (1) an attentionally demanding choice reaction time task (CRT); and (2) an unconstrained "rest" state. Functional MRI demonstrated increased synchrony, and decreased metastability was associated with increased activity within the frontoparietal control/dorsal attention network (FPCN/DAN) activity and decreased default mode network (DMN) activity during the CRT compared with rest. Using a computational model of neural dynamics that is constrained by white matter structure to test whether simulated changes in FPCN/DAN and DMN activity produce similar effects, we demonstate that activation of the FPCN/DAN increases global synchrony and decreases metastability. DMN activation had the opposite effects. These results suggest that the balance of activity in the FPCN/DAN and DMN might control global metastability, providing a mechanistic explanation of how attentional state is shifted between an unfocused/exploratory mode characterized by high metastability, and a focused/constrained mode characterized by low metastability.