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Critical‐like brain dynamics in a continuum from second-to first‐order phase transition
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A1 Alkuperäisartikkeli tieteellisessä aikakauslehdessä
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Journal of Neuroscience, Volume 43, issue 45, pp. 7642-7656
Abstract
The classic brain criticality hypothesis postulates that the brain benefits from operating near a continuous second‐order phase transition. Slow feedback regulation of neuronal activity could, however, lead to a discontinuous first‐order transition and thereby bistable activity. Observations of bistability in awake brain activity have nonetheless remained scarce and its functional significance unclear. Moreover, there is no empirical evidence to support the hypothesis that the human brain could flexibly operate near either a first‐ or second‐order phase transition despite such a continuum being common in models. Here, using computational modelling, we found bistable synchronization dynamics to emerge through elevated positive feedback and occur exclusively in a regime of critical‐like dynamics. We then assessed bistability in vivo with resting‐state magnetoencephalography in healthy adults (7 females, 11 males) and stereo‐electroencephalography in epilepsy patients (28 females, 36 males). This analysis revealed that a large fraction of the neocortices exhibited varying degrees of bistability in neuronal oscillations from 3 to 200 Hz. In line with our modelling results, the neuronal bistability was positively correlated with classic assessment of brain criticality across narrow‐band frequencies. Excessive bistability was predictive of epileptic pathophysiology in the patients whereas moderate bistability was positively correlated with task performance in the healthy subjects. These empirical findings thus reveal the human brain as a one‐of‐a‐kind complex system that exhibits critical‐like dynamics in a continuum between continuous and discontinuous phase transitions.
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Funding Information: The Academy of Finland SA 266402, 303933, and SA 325404 (SP) The Academy of Finland SA 253130 and 296304 (JMP) The Ella and Georg Ehrnrooth Foundation 14‐10553‐2 (SHW) Finnish Cultural Foundation 00220071 (SHW) We would like to thank our Italian collaborators from the Centre of Epilepsy Surgery “C. Munari” at Niguarda Hospital, in particular Annalisa Rubino and Dr. Francesco Cardinale, for their support. We thank Dr. James Roberts for sharing code, and Drs. Serena di Santo, Stewart Heitmann, and Alexander Zhigalov for insightful discussions. Publisher Copyright: © 2023 Society for Neuroscience. All rights reserved.
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Wang, S H, Siebenhühner, F, Arnulfo, G, Myrov, V, Nobili, L, Breakspear, M, Palva, S & Palva, J M 2023, 'Critical‐like brain dynamics in a continuum from second-to first‐order phase transition', Journal of Neuroscience, vol. 43, no. 45, pp. 7642-7656. https://doi.org/10.1523/JNEUROSCI.1889-22.2023