Distributed harmonic patterns of structure-function dependence orchestrate human consciousness

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• dc.contributor.author Luppi, Andrea I.
• dc.contributor.author Vohryzek, Jakub
• dc.contributor.author Kringelbach, Morten L.
• dc.contributor.author Martinez Mediano, Pedro Antonio
• dc.contributor.author Adapa, Ram
• dc.contributor.author Carhart-Harris, Robin L.
• dc.contributor.author Roseman, Leor
• dc.contributor.author Pappas, Ioannis
• dc.contributor.author Peattie, Alexander R. D.
• dc.contributor.author Manktelow, Anne E.
• dc.contributor.author Sahakian, Barbara J.
• dc.contributor.author Finoia, Paola
• dc.contributor.author Williams, Guy B.
• dc.contributor.author Allanson, Judith
• dc.contributor.author Pickard, John D.
• dc.contributor.author Menon, David K.
• dc.contributor.author Atasoy, Selen
• dc.contributor.author Stamatakis, Emmanuel A.
• dc.date.accessioned 2023-03-20T07:18:37Z
• dc.date.available 2023-03-20T07:18:37Z
• dc.date.issued 2023
• dc.description Supplemental material files: supplementary figures; replication files
• dc.description.abstract A central question in neuroscience is how consciousness arises from the dynamic interplay of brain structure and function. Here we decompose functional MRI signals from pathological and pharmacologically-induced perturbations of consciousness into distributed patterns of structure-function dependence across scales: the harmonic modes of the human structural connectome. We show that structure-function coupling is a generalisable indicator of consciousness that is under bi-directional neuromodulatory control. We find increased structure-function coupling across scales during loss of consciousness, whether due to anaesthesia or brain injury, capable of discriminating between behaviourally indistinguishable sub-categories of brain-injured patients, tracking the presence of covert consciousness. The opposite harmonic signature characterises the altered state induced by LSD or ketamine, reflecting psychedelic-induced decoupling of brain function from structure and correlating with physiological and subjective scores. Overall, connectome harmonic decomposition reveals how neuromodulation and the network architecture of the human connectome jointly shape consciousness and distributed functional activation across scales.
• dc.description.sponsorship This work was supported by grants from The Wellcome Trust Research Training Fellowship (grant no. 083660/Z/07/Z), Raymond and Beverly Sackler Studentship, and the Cambridge Commonwealth Trust [R.A.]; the UK Medical Research Council (U.1055.01.002.00001.01) [J.D.P.]; The James S. McDonnell Foundation [J.D.P.]; the Canadian Institute for Advanced Research (CIFAR; grant RCZB/072 RG93193) [to D.K.M. and E.A.S.]; The National Institute for Health Research (NIHR, UK), Cambridge Biomedical Research Centre and NIHR Senior Investigator Awards [J.D.P. and D.K.M.]; The British Oxygen Professorship of the Royal College of Anaesthetists [D.K.M.]; The Stephen Erskine Fellowship, Queens’ College, University of Cambridge [E.A.S.]; The Evelyn Trust, Cambridge and the EoE CLAHRC fellowship [J.A.]; The Gates Cambridge Trust [A.I.L.]; The Cambridge International Trust and the Howard Sidney Sussex Studentship [M.M.C.]; The Oon Khye Beng Ch’Hia Tsio Studentship for Research in Preventive Medicine, Downing College, University of Cambridge [I.P.]; The Wellcome Trust (grant no. 210920/Z/18/Z) [P.A.M.M.]; The European Research Council Consolidator Grant CAREGIVING (615539) [M.L.K. and S.A.]; The Center for Music in the Brain, funded by the Danish National Research Foundation (DNRF117) [M.L.K., S.A. and J.V.]; The Centre for Eudaimonia and Human Flourishing, funded by the Pettit and Carlsberg Foundations [M.L.K.]; The Imperial College President’s Scholarship [L.R.]; The Alex Mosley Charitable Trust [R.L.C.H.]; The ketamine study was funded by the Bernard Wolfe Health Neuroscience Fund and the Wellcome Trust. The original LSD study received support from a Crowd Funding Campaign and the Beckley Foundation, as part of the Beckley-Imperial Research Programme. The research was also supported by the NIHR Brain Injury Healthcare Technology Co-operative based at Cambridge University Hospitals NHS Foundation Trust and University of Cambridge. Data used to obtain the human connectome were provided by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research; and by the McDonnell Center for Systems Neuroscience at Washington University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
• dc.format.mimetype application/pdf
• dc.identifier.citation Luppi AI, Vohryzek J, Kringelbach ML, Mediano PA, Craig MM, Adapa R, et al. Distributed harmonic patterns of structure-function dependence orchestrate human consciousness. Commun Biol. 2023;18(1):2165321. DOI: 10.1038/s42003-023-04474-1
• dc.identifier.doi http://dx.doi.org/10.1038/s42003-023-04474-1
• dc.identifier.issn 2399-3642
• dc.identifier.uri http://hdl.handle.net/10230/56263
• dc.language.iso eng
• dc.publisher Nature Research
• dc.relation.ispartof Communications Biology. 2023 Jan 28;6:117
• dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/615539
• dc.rights 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 Consciousness
• dc.subject.keyword Dynamical systems
• dc.subject.keyword Network models
• dc.title Distributed harmonic patterns of structure-function dependence orchestrate human consciousness
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion