Author Summary This study demonstrates that sensorimotor behavior can be accurately predicted from single-trial EEG oscillations that exhibit coordinated fluctuations across various brain regions, frequency bands, and movement time epochs. We introduce high-dimensional oscillatory portraits to capture the relationships among basic oscillatory elements, quantifying oscillations at specific frequencies and times during individual trials. Our findings indicate that the overall structure of these interdependence networks, or effective connectivity, remains stable across different task conditions, showcasing an intrinsic coordination architecture that adapts to task constraints through subtle topological changes. Additionally, fluctuations in single-trial oscillatory portraits can predict variations in movement kinematics, with movement accuracy reflecting the oscillatory architecture’s ability to adapt in response to movement errors.

Spontaneous activity during the resting state, tracked by BOLD fMRI imaging, or shortly rsfMRI, gives rise to brain-wide dynamic patterns of interregional correlations, whose structured flexibility relates to cognitive performance. Here, we analyze resting-state dynamic functional connectivity (dFC) in a cohort of older adults, including amnesic mild cognitive impairment (aMCI, N = 34) and Alzheimer’s disease (AD, N = 13) patients, as well as normal control (NC, N = 16) and cognitively “supernormal” controls (SNC, N = 10) subjects. Using complementary state-based and state-free approaches, we find that resting-state fluctuations of different functional links are not independent but are constrained by high-order correlations between triplets or quadruplets of functionally connected regions. When contrasting patients with healthy subjects, we find that dFC between cingulate and other limbic regions is increasingly bursty and intermittent when ranking the four groups from SNC to NC, aMCI and AD. Furthermore, regions affected at early stages of AD pathology are less involved in higher order interactions in patient than in control groups, while pairwise interactions are not significantly reduced. Our analyses thus suggest that the spatiotemporal complexity of dFC organization is precociously degraded in AD and provides a richer window into the underlying neurobiology than time-averaged FC connections. Author Summary Brain functions emerge from the coordinated dynamics of many brain regions. Dynamic functional connectivity (dFC) analyses are a key tool to describe such dynamic complexity and have been shown to be good predictors of cognitive performance. This is particularly true in the case of Alzheimer’s disease (AD) in which an impoverished dFC could indicate compromised functional reserve due to the detrimental effects of neurodegeneration. Here we observe that in healthy aging, dFC is indeed spatiotemporally organized, as reflected by high-order correlations between multiple regions. However, in people with aMCI or AD, dFC becomes less “entangled,” more random-like, and intermittently bursty. We speculate that this degraded spatiotemporal coordination may reflect dysfunctional information processing, thus ultimately leading to worsening of cognitive deficits.

Author Summary It is generally thought that computations performed by local brain circuits rely on complex neural processes, associated with the flexible waxing and waning of cell assemblies, that is, an ensemble of cells firing in tight synchrony. Although cell assembly formation is inherently and unavoidably dynamical, it is still common to find studies in which essentially “static” approaches are used to characterize this process. In the present study, we adopt instead a temporal network approach. Avoiding usual time-averaging procedures, we reveal that hub neurons are not hardwired but that cells vary smoothly their degree of integration within the assembly core. Furthermore, our temporal network framework enables the definition of alternative possible styles of “hubness.” Some cells may share information with a multitude of other units but only in an intermittent manner, as “activists” in a flash mob. In contrast, some other cells may share information in a steadier manner, as resolute “lobbyists.” Finally, by avoiding averages over preimposed states, we show that within each global oscillatory state rich switching dynamics can take place between a repertoire of many available network states. We thus show that the temporal network framework provides a natural and effective language to rigorously describe the rich spatiotemporal patterns of information sharing instantiated by cell assembly evolution. Abstract Neural computation is associated with the emergence, reconfiguration, and dissolution of cell assemblies in the context of varying oscillatory states. Here, we describe the complex spatiotemporal dynamics of cell assemblies through temporal network formalism. We use a sliding window approach to extract sequences of networks of information sharing among single units in hippocampus and entorhinal cortex during anesthesia and study how global and node-wise functional connectivity properties evolve through time and as a function of changing global brain state (theta vs. slow-wave oscillations). First, we find that information sharing networks display, at any time, a core-periphery structure in which an integrated core of more tightly functionally interconnected units links to more loosely connected network leaves. However the units participating to the core or to the periphery substantially change across time windows, with units entering and leaving the core in a smooth way. Second, we find that discrete network states can be defined on top of this continuously ongoing liquid core-periphery reorganization. Switching between network states results in a more abrupt modification of the units belonging to the core and is only loosely linked to transitions between global oscillatory states. Third, we characterize different styles of temporal connectivity that cells can exhibit within each state of the sharing network. While inhibitory cells tend to be central, we show that, otherwise, anatomical localization only poorly influences the patterns of temporal connectivity of the different cells. Furthermore, cells can change temporal connectivity style when the network changes state. Altogether, these findings reveal that the sharing of information mediated by the intrinsic dynamics of hippocampal and entorhinal cortex cell assemblies have a rich spatiotemporal structure, which could not have been identified by more conventional time- or state-averaged analyses of functional connectivity.