Metastable neural dynamics underlies cognitive performance across multiple behavioural paradigms

Despite resting state networks being associated with a variety of cognitive abilities, it remains unclear how these local areas act in concert to express particular cognitive operations. Theoretical and empirical accounts indicate that large-scale resting state networks reconcile dual tendencies toward integration and segregation by operating in a metastable regime of their coordination dynamics. One proposal is that metastability confers important behavioural qualities by dynamically binding distributed local areas into large-scale neurocognitive entities. We tested this hypothesis by analysing fMRI data in a large cohort of healthy individuals (N=566) and comparing the metastability of the brain’s large-scale resting network architecture at rest and during the performance of several tasks. Task-based reasoning was principally characterised by high metastability in cognitive control networks and low metastability in sensory processing areas. Although metastability between resting state networks increased during task performance, cognitive ability was more closely linked to spontaneous activity. High metastability in the intrinsic connectivity of cognitive control networks was linked to novel problem solving (or fluid intelligence) but was less important in tasks relying on prior experience (or crystallised intelligence). Crucially, subjects with resting architectures similar or ‘pre-configured’ to a task-general arrangement demonstrated superior cognitive performance. Taken together, our findings support a critical linkage between the spontaneous metastability of the large-scale networks of the cerebral cortex and cognition.