Consciousness is supported by near-critical slow cortical electrodynamics
Daniel Toker, Ioannis Pappas, View ORCID ProfileJanna D. Lendner, View ORCID ProfileJoel Frohlich, View ORCID ProfileDiego M. Mateos, Suresh Muthukumaraswamy, Robin Carhart-Harris, View ORCID ProfileMichelle Paff, Paul M. Vespa, View ORCID ProfileMartin M. Monti, Friedrich T. Sommer, View ORCID ProfileRobert T. Knight, and Mark D’Esposito
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PNAS February 15, 2022 119 (7) e2024455119; https://doi.org/10.1073/pnas.2024455119
- Edited by Emery Brown, Department of Anesthesia and Critical Care, Massachusetts General Hospital, Boston, MA; received December 2, 2020; accepted December 20, 2021
What changes in the brain when we lose consciousness? One possibility is that the loss of consciousness corresponds to a transition of the brain’s electric activity away from edge-of-chaos criticality, or the knife’s edge in between stability and chaos. Recent mathematical developments have produced tools for testing this hypothesis, which we apply to cortical recordings from diverse brain states. We show that the electric activity of the cortex is indeed poised near the boundary between stability and chaos during conscious states and transitions away from this boundary during unconsciousness and that this transition disrupts cortical information processing.
Mounting evidence suggests that during conscious states, the electrodynamics of the cortex are poised near a critical point or phase transition and that this near-critical behavior supports the vast flow of information through cortical networks during conscious states. Here, we empirically identify a mathematically specific critical point near which waking cortical oscillatory dynamics operate, which is known as the edge-of-chaos critical point, or the boundary between stability and chaos. We do so by applying the recently developed modified 0-1 chaos test to electrocorticography (ECoG) and magnetoencephalography (MEG) recordings from the cortices of humans and macaques across normal waking, generalized seizure, anesthesia, and psychedelic states. Our evidence suggests that cortical information processing is disrupted during unconscious states because of a transition of low-frequency cortical electric oscillations away from this critical point; conversely, we show that psychedelics may increase the information richness of cortical activity by tuning low-frequency cortical oscillations closer to this critical point. Finally, we analyze clinical electroencephalography (EEG) recordings from patients with disorders of consciousness (DOC) and show that assessing the proximity of slow cortical oscillatory electrodynamics to the edge-of-chaos critical point may be useful as an index of consciousness in the clinical setting.