Relationship of Topology, Multiscale Phase Synchronization, and State Transitions in Human Brain Networks (original) (raw)
Related papers
Frontiers in Computational Neuroscience, 2016
Sleep, anesthesia, and coma share a number of neural features but the recovery profiles are radically different. To understand the mechanisms of reversibility of unconsciousness at the network level, we studied the conditions for gradual and abrupt transitions in conscious and anesthetized states. We hypothesized that the conditions for explosive synchronization (ES) in human brain networks would be present in the anesthetized brain just over the threshold of unconsciousness. To test this hypothesis, functional brain networks were constructed from multi-channel electroencephalogram (EEG) recordings in seven healthy subjects across conscious, unconscious, and recovery states. We analyzed four variables that are involved in facilitating ES in generic, non-biological networks: (1) correlation between node degree and frequency, (2) disassortativity (i.e., the tendency of highly-connected nodes to link with less-connected nodes, or vice versa), (3) frequency difference of coupled nodes, and (4) an inequality relationship between local and global network properties, which is referred to as the suppressive rule. We observed that the four network conditions for ES were satisfied in the unconscious state. Conditions for ES in the human brain suggest a potential mechanism for rapid recovery from the lightly-anesthetized state. This study demonstrates for the first time that the network conditions for ES, formerly shown in generic networks only, are present in empirically-derived functional brain networks. Further investigations with deep anesthesia, sleep, and coma could provide insight into the underlying causes of variability in recovery profiles of these unconscious states.
Subgraph “Backbone” Analysis of Dynamic Brain Networks during Consciousness and Anesthesia
PLoS ONE, 2013
General anesthesia significantly alters brain network connectivity. Graph-theoretical analysis has been used extensively to study static brain networks but may be limited in the study of rapidly changing brain connectivity during induction of or recovery from general anesthesia. Here we introduce a novel method to study the temporal evolution of network modules in the brain. We recorded multichannel electroencephalograms (EEG) from 18 surgical patients who underwent general anesthesia with either propofol (n = 9) or sevoflurane (n = 9). Time series data were used to reconstruct networks; each electroencephalographic channel was defined as a node and correlated activity between the channels was defined as a link. We analyzed the frequency of subgraphs in the network with a defined number of links; subgraphs with a high probability of occurrence were deemed network ''backbones.'' We analyzed the behavior of network backbones across consciousness, anesthetic induction, anesthetic maintenance, and two points of recovery. Constitutive, variable and state-specific backbones were identified across anesthetic state transitions. Brain networks derived from neurophysiologic data can be deconstructed into network backbones that change rapidly across states of consciousness. This technique enabled a granular description of network evolution over time. The concept of network backbones may facilitate graph-theoretical analysis of dynamically changing networks.
Oscillations, criticality and responsiveness in complex brain networks
2019
Brain networks during unconscious states resulting from sleep, anesthesia, or traumatic injuries are associated with a limited capacity for complex responses to stimulation. Even during the conscious resting state, responsiveness to stimulus is highly dependent on spontaneous brain activities. Many empirical findings have been suggested that the brain responsiveness is determined mainly by the ongoing brain activity when a stimulus is given. However, there has been no systematic study exploring how such various brain activities with high or low synchronization, amplitude, and phase response to stimuli. In this model study, we simulated large-scale brain network dynamics in three brain states (below, near, and above the critical state) and investigated a relationship between ongoing oscillation properties and a stimulus decomposing the brain activity into fundamental oscillation properties (instantaneous global synchronization, amplitude, and phase). We identified specific stimulatio...
Brain Networks Maintain a Scale-free Organization across Consciousness, Anesthesia, and Recovery
Anesthesiology, 2010
Background Loss of consciousness is an essential feature of general anesthesia. Although alterations of neural networks during anesthesia have been identified in the spatial domain, there has been relatively little study of temporal organization. Methods Ten healthy male volunteers were anesthetized with an induction dose of propofol on two separate occasions. The duration of network connections in the brain was analyzed by multichannel electroencephalography and the minimum spanning tree method. Entropy of the connections was calculated based on Shannon entropy. The global temporal configuration of networks was investigated by constructing the cumulative distribution function of connection times in different frequency bands and different states of consciousness. Results General anesthesia was associated with a significant reduction in the number of network connections, as well as significant alterations of their duration. These changes were most prominent in the δ bandwidth and wer...
NeuroImage
Recent modeling and empirical studies support the hypothesis that large-scale brain networks function near a critical state. Similar functional connectivity patterns derived from resting state empirical data and brain network models at criticality provide further support. However, despite the strong implication of a relationship, there has been no principled explanation of how criticality shapes the characteristic functional connectivity in large-scale brain networks. Here, we hypothesized that the network science concept of partial phase locking is the underlying mechanism of optimal functional connectivity in the resting state. We further hypothesized that the characteristic connectivity of the critical state provides a theoretical boundary to quantify how far pharmacologically or pathologically perturbed brain connectivity deviates from its critical state, which could enable the differentiation of various states of consciousness with a theory-based metric. To test the hypothesis, we used a neuroanatomically informed brain network model with the resulting source signals projected to electroencephalogram (EEG)-like sensor signals with a forward model. Phase lag entropy (PLE), a measure of phase relation diversity, was estimated and the topography of PLE was analyzed. To measure the distance from criticality, the PLE topography at a critical state was compared with those of the EEG data from baseline consciousness, isoflurane anesthesia, ketamine anesthesia, vegetative state/unresponsive wakefulness syndrome, and minimally conscious state. We demonstrate that the partial phase locking at criticality shapes the functional connectivity and asymmetric anterior-posterior PLE topography, with low (high) PLE for high (low) degree nodes. The topographical similarity and the strength of PLE differentiates various pharmacologic and pathologic states of consciousness. Moreover, this model-based EEG network analysis provides a novel metric to quantify how far a pharmacologically or pathologically perturbed brain network is away from critical state, rather than merely determining whether it is in a critical or non-critical state.
PLOS Computational Biology, 2018
Hysteresis, the discrepancy in forward and reverse pathways of state transitions, is observed during changing levels of consciousness. Identifying the underlying mechanism of hysteresis phenomena in the brain will enhance the ability to understand, monitor, and control state transitions related to consciousness. We hypothesized that hysteresis in brain networks shares the same underlying mechanism of hysteresis as other biological and nonbiological networks. In particular, we hypothesized that the principle of explosive synchronization, which can mediate abrupt state transitions, would be critical to explaining hysteresis in the brain during conscious state transitions. We analyzed high-density electroencephalogram (EEG) that was acquired in healthy human volunteers during conscious state transitions induced by the general anesthetics sevoflurane or ketamine. We developed a novel method to monitor the temporal evolution of EEG networks in a parameter space, which consists of the strength and topography of EEG-based networks. Furthermore, we studied conditions of explosive synchronization in anatomically informed human brain network models. We identified hysteresis in the trajectory of functional brain networks during state transitions. The model study and empirical data analysis explained various hysteresis phenomena during the loss and recovery of consciousness in a principled way: (1) more potent anesthetics induce a larger hysteresis; (2) a larger range of EEG frequencies facilitates transitions into unconsciousness and impedes the return of consciousness; (3) hysteresis of connectivity is larger than that of EEG power; and (4) the structure and strength of functional brain networks reconfigure differently during the loss vs. recovery of consciousness. We conclude that the hysteresis phenomena observed during the loss and recovery of consciousness are generic network features. Furthermore, the state transitions are grounded in the same principle as state transitions in complex non-biological networks, especially during perturbation. These findings suggest the possibility of predicting and modulating hysteresis of conscious state transitions in large-scale brain networks.
Dissociable Network Properties of Anesthetic State Transitions
Anesthesiology, 2011
Background It is still unknown whether anesthetic state transitions are continuous or binary. Mathematical graph theory is one method by which to assess whether brain networks change gradually or abruptly upon anesthetic induction and emergence. Methods Twenty healthy males were anesthetized with an induction dose of propofol, with continuous measurement of 21-channel electroencephalogram at baseline, during anesthesia, and during recovery. From these electroencephalographic data a "genuine network" was reconstructed based on the surrogate data method. The effects of topologic structure and connection strength on information transfer through the network were measured independently across different states. Results Loss of consciousness was consistently associated with a disruption of network topology. However, recovery of consciousness was associated with complex patterns of altered connection strength after the initial topologic structure had slowly recovered. In one group...
Partial synchronization in empirical brain networks as a model for unihemispheric sleep
EPL (Europhysics Letters), 2019
We analyze partial synchronization patterns in a network of FitzHugh-Nagumo oscillators with empirical structural connectivity measured in healthy human subjects. We report a dynamical asymmetry between the hemispheres, induced by the natural structural asymmetry. We show that the dynamical asymmetry can be enhanced by introducing the inter-hemispheric coupling strength as a control parameter for partial synchronization patterns. We specify the possible modalities for existence of unihemispheric sleep in human brain, where one hemisphere sleeps while the other remains awake. In fact, this state is common among migratory birds and mammals like aquatic species.
bioRxiv (Cold Spring Harbor Laboratory), 2020
Understanding the many facets of the organization of brain dynamics at large scales remains largely unexplored. Here, we construct a brain-wide model based on recent progress in biologically-realistic population models obtained using mean-field techniques. We use The Virtual Brain (TVB) as a simulation platform and incorporate mean-field models of networks of Adaptive Exponential (AdEx) integrate-and-fire neurons. Such models can capture the main intrinsic firing properties of central neurons, such as adaptation, and also include the typical kinetics of postsynaptic conductances. We hypothesize that such features are important to a biologically realistic simulation of brain dynamics. The resulting "TVB-AdEx" model is shown here to generate two fundamental dynamical states, asynchronous-irregular (AI) and Up-Down states, which correspond to the asynchronous and synchronized dynamics of wakefulness and slow-wave sleep, respectively. The synchrony of slow waves appear as an emergent property at large scales, and reproduce the very different patterns of functional connectivity found in slow-waves compared to asynchronous states. Next, we simulated experiments with transcranial magnetic stimulation (TMS) during asynchronous and slow-wave states, and show that, like in experimental data, the effect of the stimulation greatly depends on the activity state. During slow waves, the response is strong but remains local, in contrast with asynchronous states, where the response is weaker but propagates across brain areas. To compare more quantitatively with wake and slow-wave sleep states, we compute the perturbational complexity index and show that it matches the value estimated from TMS experiments. We conclude that the TVB-AdEx model replicates some of the properties of synchrony and responsiveness seen in the human brain, and is a promising tool to study spontaneous and evoked large-scale dynamics in the normal, anesthetized or pathological brain.
Brain network motifs are markers of loss and recovery of consciousness
Motifs are patterns of inter-connections between nodes of a network, and have been investigated as building blocks of directed networks. This study explored the re-organization of 3-node motifs during loss and recovery of consciousness. Nine healthy subjects underwent a 3-hour anesthetic protocol while 128-channel electroencephalography (EEG) was recorded. In the alpha (8–13 Hz) band, five-minute epochs of EEG were extracted for: baseline; induction; unconsciousness; 30-, 10- and 5-minutes pre-recovery of consciousness; 30- and 180-minutes post-recovery of consciousness. We constructed a functional brain network using both the weighted and the directed phase lag index, on which we calculated graph theoretical network properties, and the frequency and topography of 3-node motifs. Three motifs (motifs 1, 2 and 5) were significantly present across participants and epochs, when compared to random networks (p<0.05). While graph theoretical properties varied inconsistently across uncon...