Metastable oscillatory modes emerge from synchronization in the brain spacetime connectome

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• dc.contributor.author Cabral, Joana
• dc.contributor.author Castaldo, Francesca
• dc.contributor.author Vohryzek, Jakub
• dc.contributor.author Litvak, Vladimir
• dc.contributor.author Bick, Christian
• dc.contributor.author Lambiotte, Renaud
• dc.contributor.author Friston, Karl
• dc.contributor.author Kringelbach, Morten L.
• dc.contributor.author Deco, Gustavo
• dc.date.accessioned 2023-03-06T07:30:24Z
• dc.date.available 2023-03-06T07:30:24Z
• dc.date.issued 2022
• dc.description.abstract A rich repertoire of oscillatory signals is detected from human brains with electro- and magnetoencephalography (EEG/MEG). However, the principles underwriting coherent oscillations and their link with neural activity remain under debate. Here, we revisit the mechanistic hypothesis that transient brain rhythms are a signature of metastable synchronization, occurring at reduced collective frequencies due to delays between brain areas. We consider a system of damped oscillators in the presence of background noise – approximating the short-lived gamma-frequency oscillations generated within neuronal circuits – coupled according to the diffusion weighted tractography between brain areas. Varying the global coupling strength and conduction speed, we identify a critical regime where spatially and spectrally resolved metastable oscillatory modes (MOMs) emerge at sub-gamma frequencies, approximating the MEG power spectra from 89 healthy individuals at rest. Further, we demonstrate that the frequency, duration, and scale of MOMs – as well as the frequency-specific envelope functional connectivity – can be controlled by global parameters, while the connectome structure remains unchanged. Grounded in the physics of delay-coupled oscillators, these numerical analyses demonstrate how interactions between locally generated fast oscillations in the connectome spacetime structure can lead to the emergence of collective brain rhythms organized in space and time.
• dc.description.sponsorship J.C. is funded by the Portuguese Foundation for Science and Technology grants UIDB/50026/2020, UIDP/50026/2020 and CEECIND/03325/2017, Portugal. F.C. is funded by the EU-project euSNN European School of Network Neuroscience (MSCA-ITN-ETN H2020-860563). The Wellcome Centre for Human Neuroimaging is supported by core funding from Wellcome [203147/Z/16/Z]. J.V. is supported by the EU H2020 FET Proactive project Neurotwin grant agreement no. 101017716. R.L. acknowledges support from EPRSC Grants No. EP/V013068/1 and EP/V03474X/1. C.B. acknowledges support from the Engineering and Physical Sciences Research Council (EPSRC) through the grant EP/T013613/1. MLK is supported by the Center for Music in the Brain, funded by the Danish National Research Foundation (DNRF117), and the Centre for Eudaimonia and Human Flourishing, funded by the Pettit Foundation and Carlsberg Foundation. G.D. is supported by the Spanish national research project (PID2019-105772GB-I00 MCIU AEI), funded by the Spanish Ministry of Science, Innovation and Universities (MCIU), State Research Agency (AEI); HBP SGA3 Human Brain Project Specific grant agreement 3 (945539), funded by the EU H2020 FET Flagship program; SGR Research Support Group (reference 2017 SGR 1545), funded by the Catalan Agency for Management of University and Research Grants (AGAUR); Neurotwin Digital twins for model-driven non-invasive electrical brain stimulation (grant agreement 101017716), funded by the EU H2020 FET Proactive program; euSNN (grant agreement 860563), funded by the EU H2020 MSCA-ITN Innovative Training Networks; The Emerging Human Brain Cluster (CECH) (001-P-001682) within the framework of the European Research Development Fund Operational Program of Catalonia 2014–2020; Brain-Connects: Brain Connectivity during Stroke Recovery and Rehabilitation (201725.33), funded by the Fundacio La Marato TV3; and Corticity, FLAG-ERA JTC 2017 (reference PCI2018-092891), funded by the MCIU, AEI.
• dc.format.mimetype application/pdf
• dc.identifier.citation Cabral J, Castaldo F, Vohryzek J, Litvak V, Bick C, Lambiotte R, Friston K, Kringelbach ML, Deco G. Metastable oscillatory modes emerge from synchronization in the brain spacetime connectome. Commun Phys. 2022;5:184. DOI: 10.1038/s42005-022-00950-y
• dc.identifier.doi http://dx.doi.org/10.1038/s42005-022-00950-y
• dc.identifier.issn 2399-3650
• dc.identifier.uri http://hdl.handle.net/10230/56050
• dc.language.iso eng
• dc.publisher Nature Research
• dc.relation.ispartof Communications Physics. 2022;5:184.
• dc.relation.isreferencedby https://github.com/fcast7/Hopf_Delay_Toolbox
• dc.relation.isreferencedby https://static-content.springer.com/esm/art%3A10.1038%2Fs42005-022-00950-y/MediaObjects/42005_2022_950_MOESM1_ESM.pdf
• dc.relation.isreferencedby https://static-content.springer.com/esm/art%3A10.1038%2Fs42005-022-00950-y/MediaObjects/42005_2022_950_MOESM2_ESM.pdf
• dc.relation.isreferencedby https://static-content.springer.com/esm/art%3A10.1038%2Fs42005-022-00950-y/MediaObjects/42005_2022_950_MOESM3_ESM.docx
• dc.relation.isreferencedby https://static-content.springer.com/esm/art%3A10.1038%2Fs42005-022-00950-y/MediaObjects/42005_2022_950_MOESM4_ESM.mov
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/860563
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/945539
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/101017716
• dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PCI2018-092891
• dc.relation.projectID info:eu-repo/grantAgreement/ES/2PE/PID2019-105772GB-I00
• dc.rights © The Author(s) 2022. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/ licenses/by/4.0/.
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by/4.0/
• dc.subject.keyword Complex networks
• dc.subject.keyword Computational biophysics
• dc.subject.keyword Nonlinear phenomena
• dc.subject.keyword Phase transitions and critical phenomena
• dc.title Metastable oscillatory modes emerge from synchronization in the brain spacetime connectome
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion