Synchrony, metastability, dynamic integration, and competition in the spontaneous functional connectivity of the human brain

Available online 3 June 2019.The human brain is functionally organized into large-scale neural networks that are dynamically interconnected. Multiple short-lived states of resting-state functional connectivity (rsFC) identified transiently synchronized networks and cross-network integration. However, little is known about the way brain couplings covary as rsFC states wax and wane. In this magnetoencephalography study, we explore the synchronization structure among the spontaneous interactions of well-known resting-state networks (RSNs). To do so, we extracted modes of dynamic coupling that reflect rsFC synchrony and analyzed their spatio-temporal features. These modes identified transient, sporadic rsFC changes characterized by the widespread integration of RSNs across the brain, most prominently in the β band. This is in line with the metastable rsFC state model of resting-state dynamics, wherein our modes fit as state transition processes. Furthermore, the default-mode network (DMN) stood out as being structured into competitive cross-network couplings with widespread DMN-RSN interactions, especially among the β-band modes. These results substantiate the theory that the DMN is a core network enabling dynamic global brain integration in the β band.This work was supported by the Action de Recherche Concert ee (ARC Consolidation 2015–2019, “Characterization of the electrophysiological bases, the temporal dynamics and the functional relevance of resting state network” attributed to X.D.T.) and by the research convention “Les Voies du Savoir” (Fonds Erasme, Brussels, Belgium). M.B. benefited from the program Attract of Innoviris (grant 2015-BB2B-10), the Spanish Ministry of Economy and Competitiveness (grant PSI2016-77175-P), and theMarie Skłodowska-Curie Action of the European Commission (grant 743562). M.V.G. and G.N.were supported by the Fonds Erasme. N.C. benefited from a research grant from the ARC Consolidation (2014–2017, “Characterization of the electrophysiological bases, the temporal dynamics and the functional relevance of resting state network” attributed to X.D.T.) and from the Fonds Erasme (research convention “Les Voies du Savoir”). X.D.T. is Post-doctorate Clinical Master Specialist at the Fonds de la Recherche Scientifique (F.R.S.-FNRS, Brussels, Belgium). The MEG project at the CUB – H^opital Erasme is financially supported by the Fonds Erasme (research convention “Les Voies du Savoir”)

Module hierarchy and centralisation in the anatomy and dynamics of human cortex

Systems neuroscience has recently unveiled numerous fundamental features of the macroscopic architecture of the human brain, the connectome, and we are beginning to understand how characteristics of brain dynamics emerge from the underlying anatomical connectivity. The current work utilises complex network analysis on a high-resolution structural connectivity of the human cortex to identify generic organisation principles, such as centralised, modular and hierarchical properties, as well as specific areas that are pivotal in shaping cortical dynamics and function. After confirming its small-world and modular architecture, we characterise the cortex’ multilevel modular hierarchy, which appears to be reasonably centralised towards the brain’s strong global structural core. The potential functional importance of the core and hub regions is assessed by various complex network metrics, such as integration measures, network vulnerability and motif spectrum analysis. Dynamics facilitated by the large-scale cortical topology is explored by simulating coupled oscillators on the anatomical connectivity. The results indicate that cortical connectivity appears to favour high dynamical complexity over high synchronizability. Taking the ability to entrain other brain regions as a proxy for the threat posed by a potential epileptic focus in a given region, we also show that epileptic foci in topologically more central areas should pose a higher epileptic threat than foci in more peripheral areas. To assess the influence of macroscopic brain anatomy in shaping global resting state dynamics on slower time scales, we compare empirically obtained functional connectivity data with data from simulating dynamics on the structural connectivity. Despite considerable micro-scale variability between the two functional connectivities, our simulations are able to approximate the profile of the empirical functional connectivity. Our results outline the combined characteristics a hierarchically modular and reasonably centralised macroscopic architecture of the human cerebral cortex, which, through these topological attributes, appears to facilitate highly complex dynamics and fundamentally shape brain function

Oscillatory dynamics as a mechanism of integration in complex networks of neurons

The large-scale integrative mechanisms of the brain, the means by which the activity of functionally segregated neuronal regions are combined, are not well understood. There is growing agreement that a flexible mechanism of integration must be present in order to support the myriad changing cognitive demands under which we are placed. Neuronal communication through phase-coherent oscillation stands as the prominent theory of cognitive integration. The work presented in this thesis explores the role of oscillation and synchronisation in the transfer and integration of information in the brain. It is first shown that complex metastable dynamics suitable for modelling phase-coherent neuronal synchronisation emerge from modularity in networks of delay and pulse-coupled oscillators. Within a restricted parameter regime these networks display a constantly changing set of partially synchronised states where some modules remain highly synchronised while others desynchronise. An examination of network phase dynamics shows increasing coherence with increasing connectivity between modules. The metastable chimera states that emerge from the activity of modular oscillator networks are demonstrated to be synchronous with a constant phase relationship as would be required of a mechanism of large-scale neural integration. A specific example of functional phase-coherent synchronisation within a spiking neural system is then developed. Competitive stimulus selection between converging population encoded stimuli is demonstrated through entrainment of oscillation in receiving neurons. The behaviour of the model is shown to be analogous to well-known competitive processes of stimulus selection such as binocular rivalry, matching key experimentally observed properties for the distribution and correlation of periods of entrainment under differing stimuli strength. Finally two new measures of network centrality, knotty-centrality and set betweenness centrality, are developed and applied to empirically derived human structural brain connectivity data. It is shown that human brain organisation exhibits a topologically central core network within a modular structure consistent with the generation of synchronous oscillation with functional phase dynamics

Metastability: an emergent phenomenon in networks of spiking neurons

It is widely recognised that different brain areas perform different specialised functions. However, it remains an open question how different brain areas coordinate with each other and give rise to global brain states and high-level cognition. Recent theories suggest that transient periods of synchronisation and desynchronisation provide a mechanism for dynamically integrating and forming coalitions of functionally related neural areas, and that at these times conditions are optimal for information transfer. Empirical evidence from human resting state networks has shown a tendency for multiple brain areas to synchronise for short amounts of time, and for different synchronous groups to appear at different times. In dynamical systems terms, this behaviour resembles metastability — an intrinsically driven movement between transient, attractor-like states. However, it remains an open question what the underlying mechanism is that gives rise to these observed phenomena. The thesis first establishes that oscillating neural populations display a great amount of spectral complexity, with several rhythms temporally coexisting in the same and different structures. The thesis next explores inter-band frequency modulation between neural oscillators. The results show that oscillations in different neural populations, and in different frequency bands, modulate each other so as to change frequency. Further to this, the interaction of these fluctuating frequencies in the network as a whole is able to drive different neural populations towards episodes of synchrony. Finally, a symbiotic relationship between metastability and underlying network structure is elucidated, in which the presence of plasticity, responding to the interactions between different neural areas, will naturally form modular small-world networks that in turn further promote metastability. This seemingly inevitable drive towards metastabilty in simulation suggests that it should also be present in biological brains. The conclusion drawn is that these key network characteristics, and the metastable dynamics they promote, facilitate versatile exploration, integration, and communication between functionally related neural areas, and thereby support sophisticated cognitive processing in the brain.Open Acces