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Critical dynamics in spontaneous EEG predict anesthetic-induced loss of consciousness and perturbational complexity.

Charlotte Maschke, Jordan O'Byrne, Michele Angelo Colombo, Melanie Boly, Olivia Gosseries, Steven Laureys, Mario Rosanova, Karim Jerbi, Stefanie Blain-Moraes

Communications biology August 5, 2024 DOI: 10.1038/s42003-024-06613-8 via PubMed

Summary

Consciousness may depend on brain activity poised at criticality—a state with complex patterns and high sensitivity to disruption. Analyzing resting-state EEG from healthy volunteers under propofol, xenon, or ketamine anesthesia, the study found that unconsciousness (from propofol or xenon) shifted brain dynamics away from avalanche criticality and the edge of chaos. Ketamine anesthesia preserved consciousness (vivid dreams) and criticality. Dynamical properties from resting EEG accurately predicted individual values of the perturbational complexity index (PCI), a TMS-based consciousness measure. The findings link perturbational complexity to criticality and suggest criticality is necessary for consciousness.

Study at a glance

Characteristics Observational cohort Peer reviewed
Population Healthy subjects undergoing general anesthesia
Keywords Neuroscience Consciousness Brain-states Anesthesia Critical-systems
Citations 50
Key finding States of unconsciousness are characterized by a distancing from avalanche criticality and the edge of chaos, and resting-state EEG dynamical properties predict perturbational complexity index values.

Abstract

Consciousness has been proposed to be supported by electrophysiological patterns poised at criticality, a dynamical regime which exhibits adaptive computational properties, maximally complex patterns and divergent sensitivity to perturbation. Here, we investigate dynamical properties of the resting-state electroencephalogram (EEG) of healthy subjects undergoing general anesthesia with propofol, xenon or ketamine. Importantly, all participants were unresponsive under anesthesia, while consciousness was retained only during ketamine anesthesia (in the form of vivid dreams), enabling an experimental dissociation between unresponsiveness and unconsciousness. For each condition, we measure (i) avalanche criticality, (ii) chaoticity, and (iii) criticality-related metrics, revealing that states of unconsciousness are characterized by a distancing from both avalanche criticality and the edge of chaos. We then ask whether these same dynamical properties are predictive of the perturbational complexity index (PCI), a TMS-based measure that has shown remarkably high sensitivity in detecting consciousness independently of behavior. We successfully predict individual subjects' PCI values with considerably high accuracy from resting-state EEG dynamical properties alone. Our results establish a firm link between perturbational complexity and criticality, and provide further evidence that criticality is a necessary condition for the emergence of consciousness.

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