Investigations of the human brain's connectomic architecture have produced two alternative models: one describes the brain's spatial structure in terms of static localized networks, and the other describes the brain's temporal structure in terms of dynamic whole-brain states. Here, we used tools from connectivity dynamics to develop a synthesis that bridges these models. Using resting fMRI data, we investigated the assumptions undergirding current models of the human connectome. Consistent with state-based models, our results suggest that static localized networks are superordinate approximations of underlying dynamic states. Furthermore, each of these localized, dynamic connectivity states is associated with global changes in the whole-brain functional connectome. By nesting localized dynamic connectivity states within their whole-brain contexts, we demonstrate the relative temporal independence of brain networks. Our assay for functional autonomy of coordinated neural systems is broadly applicable, and our findings provide evidence of structure in temporal state dynamics that complements the well-described static spatial organization of the brain.A major endeavor in neuroscience is to characterize the spatiotemporal organization of the brain into functional systems 1 . By identifying patterns of synchronous brain activity, functional magnetic resonance neuroimaging (fMRI) techniques have partitioned the human brain into large-scale networks 2,3 . These functional networks are stable across individuals and populations [4][5][6] , are roughly consistent across task-evoked and resting data 7,8 , and are present across mammalian species 9, 10 . A hierarchically modularized set of canonical networks is now widely accepted as an organizational principle of the brain 11,12 . Indeed, an expanding literature relates networks to specific psychological functions and individual differences [13][14][15][16] , with the potential for improved clinical diagnosis or treatment outcome metrics [17][18][19] . However, a growing body of work has called into question how accurately this canonical network model represents underlying neural architecture. In particular, many methods used to delineate networks rely on two implicit assumptions. First is the 'spatial assumption' that each brain region participates in exactly one network. Casting doubt on this are models suggesting that brain regions can engage with several different networks [20][21][22][23][24][25][26] , dynamic causal models showing that connectivity between brain regions changes as a function of the experimental context 27 , and graph theoretic models intimating the existence of neural hubs that recruit multiple networks [28][29][30][31] . Second is the 'temporal assumption' that the connectivity within each network remains relatively stable over time. This, too, has been called into question, with recent work 32 suggesting that the brain is dynamically multistable. That is, the brain may occupy any of a number of connectivity states over time, each with a distinct ne...