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Critical-like bistable dynamics in the resting-state human brain

View ORCID ProfileSheng H. Wang, View ORCID ProfileGabriele Arnulfo, View ORCID ProfileVladislav Myrov, View ORCID ProfileFelix Siebenhühner, Lino Nobili, View ORCID ProfileMichael Breakspear, View ORCID ProfileSatu Palva, View ORCID ProfileJ. Matias Palva
doi: https://doi.org/10.1101/2022.01.09.475554
Sheng H. Wang
1Neuroscience Center, Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Finland
2Doctoral Programme Brain & Mind, University of Helsinki, Finland
3BioMag laboratory, HUS Medical Imaging Center, Helsinki, Finland
4Department of Neuroscience and Biomedical Engineering, Aalto University, Finland
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  • For correspondence: sheng.wang@helsinki.fi matias.palva@helsinki.fi
Gabriele Arnulfo
1Neuroscience Center, Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Finland
5Department of Informatics, Bioengineering, Robotics and System engineering, University of Genoa, Genoa, Italy
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Vladislav Myrov
1Neuroscience Center, Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Finland
4Department of Neuroscience and Biomedical Engineering, Aalto University, Finland
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Felix Siebenhühner
1Neuroscience Center, Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Finland
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Lino Nobili
6Department of Neurosciences, Rehabilitation, Ophthalmology, Genetics and Maternal and Children’s Sciences, University of Genoa, Genoa, Italy
7Child Neuropsychiatry Unit, IRCCS Istituto Giannina Gaslini, Genoa, Italy
8Centre of Epilepsy Surgery “C. Munari”, Department of Neuroscience, Niguarda Hospital, Milan, Italy
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Michael Breakspear
9College of Engineering, Science and Environment; College of Health and Medicine, University of Newcastle, Callaghan, Australia
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  • ORCID record for Michael Breakspear
Satu Palva
1Neuroscience Center, Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Finland
10Centre for Cognitive Neuroimaging, Institute of Neuroscience & Psychology, University of Glasgow, United Kingdom
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J. Matias Palva
1Neuroscience Center, Helsinki Institute of Life Science (HiLIFE), University of Helsinki, Finland
4Department of Neuroscience and Biomedical Engineering, Aalto University, Finland
10Centre for Cognitive Neuroimaging, Institute of Neuroscience & Psychology, University of Glasgow, United Kingdom
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  • For correspondence: sheng.wang@helsinki.fi matias.palva@helsinki.fi
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Abstract

Brain activity exhibits scale-free avalanche dynamics and power-law long-range temporal correlations (LRTCs) across the nervous system. This has been thought to reflect “brain criticality”, i.e., brains operating near a critical phase transition between disorder and excessive order. Neuronal activity is, however, metabolically costly and may be constrained by activity-limiting mechanisms and resource depletion, which could make the phase transition discontinuous and bistable. Observations of bistability in awake human brain activity have nonetheless remained scarce and its functional significance unclear. First, using computational modelling where bistable synchronization dynamics emerged through local positive feedback, we found bistability to occur exclusively in a regime of critical-like dynamics. We then assessed bistability in vivo with resting-state magnetoencephalography and stereo-encephalography. Bistability was a robust characteristic of cortical oscillations throughout frequency bands from δ (3-7 Hz) to high-γ (100-225 Hz). As predicted by modelling, bistability and LRTCs were positively correlated. Importantly, while moderate levels of bistability were positively correlated with executive functioning, excessive bistability was associated with epileptic pathophysiology and predictive of local epileptogenicity. Critical bistability is thus a salient feature of spontaneous human brain dynamics in awake resting-state and is both functionally and clinically significant. These findings expand the framework of brain criticality and show that critical-like neuronal dynamics in vivo involves both continuous and discontinuous phase transitions in a frequency-, neuroanatomy-, and state-dependent manner.

Competing Interest Statement

The authors have declared no competing interest.

  • Abbreviations

    BiS
    bistability index
    DFA
    the scaling exponent obtained with detrended fluctuation analysis is an estimate of LTRCs
    EZ
    epileptogenic zone
    nEZ
    non-EZ, areas outside of the epileptogenic zone
    κ
    coupling strength between oscillators in the Kuramoto model
    LRTCs
    long-range temporal correlations
    MEG
    magnetoencephalography
    ρ
    the strength of the state-dependent noise in the Kuramoto model
    R
    the order parameter of the Kuramoto model
    SEEG
    stereo-EEG
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    Posted January 10, 2022.
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    Critical-like bistable dynamics in the resting-state human brain
    Sheng H. Wang, Gabriele Arnulfo, Vladislav Myrov, Felix Siebenhühner, Lino Nobili, Michael Breakspear, Satu Palva, J. Matias Palva
    bioRxiv 2022.01.09.475554; doi: https://doi.org/10.1101/2022.01.09.475554
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    Critical-like bistable dynamics in the resting-state human brain
    Sheng H. Wang, Gabriele Arnulfo, Vladislav Myrov, Felix Siebenhühner, Lino Nobili, Michael Breakspear, Satu Palva, J. Matias Palva
    bioRxiv 2022.01.09.475554; doi: https://doi.org/10.1101/2022.01.09.475554

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