Abstract
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 non-biological 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.
Highlights
Hysteresis, the differential pathway of forward and reverse state transitions, is a universal phenomenon observed in nature and has been investigated in various fields such as physics, engineering, biology, and economics[1,2,3,4,5,6,7,8,9,10,11,12]
To identify empirical evidence of hysteresis based on EEG, we examined the EEG networks during the loss and recovery of consciousness induced by anesthesia
The change of topographic similarity indicates how the connectivity structure changes during general anesthesia compared to the baseline state
Summary
Hysteresis, the differential pathway of forward and reverse state transitions, is a universal phenomenon observed in nature and has been investigated in various fields such as physics, engineering, biology, and economics[1,2,3,4,5,6,7,8,9,10,11,12]. Hysteresis has been observed during state transitions in the brain, such as sleep[6,7] and general anesthesia[8,9,10,11,12]. It has been found in both drosophila and murine models that the concentration of general anesthetic required to induce unconsciousness is higher than the concentration at which consciousness is regained. Neural inertia suggests that hysteresis is not a pharmacokinetic attribute, but a fundamental neurobiological process that stabilizes states of consciousness and creates resistance to rapid and potentially catastrophic transitions [8]. If hysteresis is a large-scale network phenomenon in the brain like many other biological and physical systems, the state transitions may be governed by the same network mechanism, which is referred to as ‘explosive synchronization.’
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