Rich-club connectivity, diverse population coupling, and dynamical activity patterns emerging from local cortical circuits

Experimental studies have begun revealing essential properties of the structural connectivity and the spatiotemporal activity dynamics of cortical circuits. To integrate these properties from anatomy and physiology, and to elucidate the links between them, we develop a novel cortical circuit model that captures a range of realistic features of synaptic connectivity. We show that the model accounts for the emergence of higher-order connectivity structures, including highly connected hub neurons that form an interconnected rich-club. The circuit model exhibits a rich repertoire of dynamical activity states, ranging from asynchronous to localized and global propagating wave states. We find that around the transition between asynchronous and localized propagating wave states, our model quantitatively reproduces a variety of major empirical findings regarding neural spatiotemporal dynamics, which otherwise remain disjointed in existing studies. These dynamics include diverse coupling (correlation) between spiking activity of individual neurons and the population, dynamical wave patterns with variable speeds and precise temporal structures of neural spikes. We further illustrate how these neural dynamics are related to the connectivity properties by analysing structural contributions to variable spiking dynamics and by showing that the rich-club structure is related to the diverse population coupling. These findings establish an integrated account of structural connectivity and activity dynamics of local cortical circuits, and provide new insights into understanding their working mechanisms. Author summary To integrate essential anatomical and physiological properties of local cortical circuits and to elucidate mechanistic links between them, we develop a novel circuit model capturing key synaptic connectivity features. We show that the model explains the emergence of a range of connectivity patterns such as rich-club connectivity, and gives rise to a rich repertoire of cortical states. We identify both the anatomical and physiological mechanisms underlying the transition of these cortical states, and show that our model reconciles an otherwise disparate set of key physiological findings on neural activity dynamics. We further illustrate how these neural dynamics are related to the connectivity properties by analysing structural contributions to variable spiking dynamics and by showing that the rich-club structure is related to diverse neural population correlations as observed recently. Our model thus provides a framework for integrating and explaining a variety of neural connectivity properties and spatiotemporal activity dynamics observed in experimental studies, and provides novel experimentally testable predictions.