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Dynamic core-periphery structure of information sharing networks in entorhinal cortex and hippocampus
Publisher: Journals Gateway
Network Neuroscience (2020) 4 (3): 946–975.
Published: 01 September 2020
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AbstractView article PDF
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. 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.
Includes: Supplementary data