Low-dimensional organization of global brain states of reduced consciousness

Yonatan Sanz Perl; Carla Pallavicini; Juan Piccinini; Athena Demertzi; Vincent Bonhomme; Charlotte Martial; Rajanikant Panda; Naji Alnagger; Jitka Annen; Olivia Gosseries; Agustin Ibañez; Helmut Laufs; Jacobo D. Sitt; Viktor K. Jirsa; Morten L. Kringelbach; Steven Laureys; Gustavo Deco; Enzo Tagliazucchi

doi:10.1016/j.celrep.2023.112491

Low-dimensional organization of global brain states of reduced consciousness

Yonatan Sanz Perl, Carla Pallavicini, Juan Piccinini, Athena Demertzi, Vincent Bonhomme, Charlotte Martial, Rajanikant Panda, Naji Alnagger, Jitka Annen, Olivia Gosseries, Agustin Ibañez, Helmut Laufs, Jacobo D. Sitt, Viktor K. Jirsa, Morten L. Kringelbach, Steven Laureys, Gustavo Deco, Enzo Tagliazucchi

Research output: Contribution to journal › Article › peer-review

1 Scopus citations

Abstract

Brain states are frequently represented using a unidimensional scale measuring the richness of subjective experience (level of consciousness). This description assumes a mapping between the high-dimensional space of whole-brain configurations and the trajectories of brain states associated with changes in consciousness, yet this mapping and its properties remain unclear. We combine whole-brain modeling, data augmentation, and deep learning for dimensionality reduction to determine a mapping representing states of consciousness in a low-dimensional space, where distances parallel similarities between states. An orderly trajectory from wakefulness to patients with brain injury is revealed in a latent space whose coordinates represent metrics related to functional modularity and structure-function coupling, increasing alongside loss of consciousness. Finally, we investigate the effects of model perturbations, providing geometrical interpretation for the stability and reversibility of states. We conclude that conscious awareness depends on functional patterns encoded as a low-dimensional trajectory within the vast space of brain configurations.

Original language	English
Article number	112491
Journal	Cell Reports
Volume	42
Issue number	5
DOIs	https://doi.org/10.1016/j.celrep.2023.112491
State	Published - 30 May 2023
Externally published	Yes

Keywords

CP: Neuroscience
deep learning
fMRI
low-dimensional brain dynamics
reduced consciousness
variational autoencoders
whole-brain modeling

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10.1016/j.celrep.2023.112491

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Perl, Y. S., Pallavicini, C., Piccinini, J., Demertzi, A., Bonhomme, V., Martial, C., Panda, R., Alnagger, N., Annen, J., Gosseries, O., Ibañez, A., Laufs, H., Sitt, J. D., Jirsa, V. K., Kringelbach, M. L., Laureys, S., Deco, G., & Tagliazucchi, E. (2023). Low-dimensional organization of global brain states of reduced consciousness. Cell Reports, 42(5), Article 112491. https://doi.org/10.1016/j.celrep.2023.112491

@article{93b7f15ffc5248d09ed45368cd268235,

title = "Low-dimensional organization of global brain states of reduced consciousness",

abstract = "Brain states are frequently represented using a unidimensional scale measuring the richness of subjective experience (level of consciousness). This description assumes a mapping between the high-dimensional space of whole-brain configurations and the trajectories of brain states associated with changes in consciousness, yet this mapping and its properties remain unclear. We combine whole-brain modeling, data augmentation, and deep learning for dimensionality reduction to determine a mapping representing states of consciousness in a low-dimensional space, where distances parallel similarities between states. An orderly trajectory from wakefulness to patients with brain injury is revealed in a latent space whose coordinates represent metrics related to functional modularity and structure-function coupling, increasing alongside loss of consciousness. Finally, we investigate the effects of model perturbations, providing geometrical interpretation for the stability and reversibility of states. We conclude that conscious awareness depends on functional patterns encoded as a low-dimensional trajectory within the vast space of brain configurations.",

keywords = "CP: Neuroscience, deep learning, fMRI, low-dimensional brain dynamics, reduced consciousness, variational autoencoders, whole-brain modeling",

author = "Perl, {Yonatan Sanz} and Carla Pallavicini and Juan Piccinini and Athena Demertzi and Vincent Bonhomme and Charlotte Martial and Rajanikant Panda and Naji Alnagger and Jitka Annen and Olivia Gosseries and Agustin Iba{\~n}ez and Helmut Laufs and Sitt, {Jacobo D.} and Jirsa, {Viktor K.} and Kringelbach, {Morten L.} and Steven Laureys and Gustavo Deco and Enzo Tagliazucchi",

note = "Funding Information: The authors thank participants and their families for their invaluable time and commitment to our study. The authors thank the whole staff from the Radiodiagnostic and Nuclear Medicine departments, University Hospital of Liege, especially Roland Hustinx, Claire Bernard, Jean-Flory Tshibanda, and Nathalie Maquet. Y.S.P. is supported by the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant 896354. E.T. is supported by PICT-2019-02294 (Agencia I+D+i, Argentina) and ANID/FONDECYT Regular 1220995 (Chile). A.I. is supported by grants from Takeda CW2680521; CONICET; FONCYT- PICT (2017-1818, 2017-1820); ANID/FONDECYT Regular (1210195, 1210176, and 1220995); ANID/FONDAP (15150012); ANID/PIA/ANILLOS ACT210096; and the Multi-Partner Consortium to Expand Dementia Research in Latin America (ReDLat), funded by the National Institutes of Aging of the National Institutes of Health under award number R01AG057234, an Alzheimer's Association grant (SG-20-725707-ReDLat), the Rainwater Foundation, and the Global Brain Health Institute (GBHI). R.P. is post-doctoral fellow, O.G. is research associate, and S.L. is research director at FRS-FNRS. The study was further supported by the University and University Hospital of Li{\`e}ge; the Belgian National Funds for Scientific Research (FRS-FNRS); the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 945539 (Human Brain Project SGA3); the FNRS PDR project (T.0134.21); the ERA-Net FLAG-ERA JTC2021 project ModelDXConsciousness (Human Brain Project Partnering Project); the fund Generet; the King Baudouin Foundation; the T{\'e}l{\'e}vie Foundation; the European Space Agency (ESA); and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Programme, the Public Utility Foundation “Universit{\'e} Europ{\'e}enne du Travail,” “Fondazione Europea Ricerca Biomedica,” the Bial Foundation, the Mind Science Foundation, the European Commission, the Fondation L{\'e}on Fredericq, the Mind-Care foundation, the DOCMA project (EU-H2020-MSCA–RISE–778234), the National Natural Science Foundation of China (Joint Research Project 81471100), and the European Foundation of Biomedical Research FERB Onlus. J.D.S. and E.T. are funded by a grant from STIC-AmSud (project SILIDOC - 21-STIC-11), ECOS-Sud A20M02, and ECOS-Sud U20S01. J.D.S. and G.D. are supported by the ModelDXConsciousness in the framework of the FLAG-ERA JTC 2021—HBP—2021 programme. E.T. is supported by PICT-2019-02294 (Agencia I+D+i, Argentina) and ANID/FONDECYT Regular 1220995 (Chile). The content of the article is solely the responsibility of the authors and does not represent the official views of these institutions. Y.S.P. A.I. M.L.K. S.L. G.D. and E.T. designed the research. Y.S.P. and E.T. conducted the research. Y.S.P. G.D. and E.T. analyzed and interpreted the results. A.D. C.M. V.B. J.D.S. J.A. O.G. N.A. R.P. H.L. and E.T. curated the data. Y.S.P. and E.T. wrote the manuscript and made figures. Y.S.P. analyzed the data. Y.S.P. G.D. and E.T. created and published the code. G.D. and E.T. supervised the research. All authors provided analytic support. All authors edited the manuscript. The authors declare no competing interests. We support inclusive, diverse, and equitable conduct of research. Funding Information: The authors thank participants and their families for their invaluable time and commitment to our study. The authors thank the whole staff from the Radiodiagnostic and Nuclear Medicine departments, University Hospital of Liege, especially Roland Hustinx, Claire Bernard, Jean-Flory Tshibanda, and Nathalie Maquet. Y.S.P. is supported by the European Union{\textquoteright}s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant 896354 . E.T. is supported by PICT - 2019-02294 (Agencia I+D+i, Argentina) and ANID / FONDECYT Regular 1220995 (Chile). A.I. is supported by grants from Takeda CW2680521 ; CONICET ; FONCYT- PICT ( 2017-1818 , 2017-1820 ); ANID / FONDECYT Regular ( 1210195 , 1210176 , and 1220995 ); ANID / FONDAP ( 15150012 ); ANID / PIA / ANILLOS ACT210096 ; and the Multi-Partner Consortium to Expand Dementia Research in Latin America (ReDLat), funded by the National Institutes of Aging of the National Institutes of Health under award number R01AG057234 , an Alzheimer's Association grant ( SG-20-725707-ReDLat ), the Rainwater Foundation , and the Global Brain Health Institute (GBHI). R.P. is post-doctoral fellow, O.G. is research associate, and S.L. is research director at FRS-FNRS. The study was further supported by the University and University Hospital of Li{\`e}ge ; the Belgian National Funds for Scientific Research (FRS-FNRS); the European Union{\textquoteright}s Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 945539 (Human Brain Project SGA3); the FNRS PDR project ( T.0134.21 ); the ERA-Net FLAG-ERA JTC2021 project ModelDXConsciousness (Human Brain Project Partnering Project); the fund Generet ; the King Baudouin Foundation ; the T{\'e}l{\'e}vie Foundation ; the European Space Agency (ESA); and the Belgian Federal Science Policy Office ( BELSPO ) in the framework of the PRODEX Programme, the Public Utility Foundation “ Universit{\'e} Europ{\'e}enne du Travail ,” “ Fondazione Europea Ricerca Biomedica ,” the Bial Foundation , the Mind Science Foundation , the European Commission , the Fondation L{\'e}on Fredericq , the Mind-Care foundation , the DOCMA project ( EU-H2020-MSCA–RISE–778234 ), the National Natural Science Foundation of China (Joint Research Project 81471100 ), and the European Foundation of Biomedical Research FERB Onlus. J.D.S. and E.T. are funded by a grant from STIC-AmSud (project SILIDOC - 21-STIC-11), ECOS-Sud A20M02, and ECOS-Sud U20S01. J.D.S. and G.D. are supported by the ModelDXConsciousness in the framework of the FLAG-ERA JTC 2021—HBP—2021 programme. E.T. is supported by PICT-2019-02294 (Agencia I+D+i, Argentina) and ANID/FONDECYT Regular 1220995 (Chile). The content of the article is solely the responsibility of the authors and does not represent the official views of these institutions. Publisher Copyright: {\textcopyright} 2023 The Authors",

year = "2023",

month = may,

day = "30",

doi = "10.1016/j.celrep.2023.112491",

language = "English",

volume = "42",

journal = "Cell Reports",

issn = "2211-1247",

publisher = "Cell Press",

number = "5",

}

Perl, YS, Pallavicini, C, Piccinini, J, Demertzi, A, Bonhomme, V, Martial, C, Panda, R, Alnagger, N, Annen, J, Gosseries, O, Ibañez, A, Laufs, H, Sitt, JD, Jirsa, VK, Kringelbach, ML, Laureys, S, Deco, G & Tagliazucchi, E 2023, 'Low-dimensional organization of global brain states of reduced consciousness', Cell Reports, vol. 42, no. 5, 112491. https://doi.org/10.1016/j.celrep.2023.112491

TY - JOUR

T1 - Low-dimensional organization of global brain states of reduced consciousness

AU - Perl, Yonatan Sanz

AU - Pallavicini, Carla

AU - Piccinini, Juan

AU - Demertzi, Athena

AU - Bonhomme, Vincent

AU - Martial, Charlotte

AU - Panda, Rajanikant

AU - Alnagger, Naji

AU - Annen, Jitka

AU - Gosseries, Olivia

AU - Ibañez, Agustin

AU - Laufs, Helmut

AU - Sitt, Jacobo D.

AU - Jirsa, Viktor K.

AU - Kringelbach, Morten L.

AU - Laureys, Steven

AU - Deco, Gustavo

AU - Tagliazucchi, Enzo

N1 - Funding Information: The authors thank participants and their families for their invaluable time and commitment to our study. The authors thank the whole staff from the Radiodiagnostic and Nuclear Medicine departments, University Hospital of Liege, especially Roland Hustinx, Claire Bernard, Jean-Flory Tshibanda, and Nathalie Maquet. Y.S.P. is supported by the European Union's Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant 896354. E.T. is supported by PICT-2019-02294 (Agencia I+D+i, Argentina) and ANID/FONDECYT Regular 1220995 (Chile). A.I. is supported by grants from Takeda CW2680521; CONICET; FONCYT- PICT (2017-1818, 2017-1820); ANID/FONDECYT Regular (1210195, 1210176, and 1220995); ANID/FONDAP (15150012); ANID/PIA/ANILLOS ACT210096; and the Multi-Partner Consortium to Expand Dementia Research in Latin America (ReDLat), funded by the National Institutes of Aging of the National Institutes of Health under award number R01AG057234, an Alzheimer's Association grant (SG-20-725707-ReDLat), the Rainwater Foundation, and the Global Brain Health Institute (GBHI). R.P. is post-doctoral fellow, O.G. is research associate, and S.L. is research director at FRS-FNRS. The study was further supported by the University and University Hospital of Liège; the Belgian National Funds for Scientific Research (FRS-FNRS); the European Union's Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 945539 (Human Brain Project SGA3); the FNRS PDR project (T.0134.21); the ERA-Net FLAG-ERA JTC2021 project ModelDXConsciousness (Human Brain Project Partnering Project); the fund Generet; the King Baudouin Foundation; the Télévie Foundation; the European Space Agency (ESA); and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Programme, the Public Utility Foundation “Université Européenne du Travail,” “Fondazione Europea Ricerca Biomedica,” the Bial Foundation, the Mind Science Foundation, the European Commission, the Fondation Léon Fredericq, the Mind-Care foundation, the DOCMA project (EU-H2020-MSCA–RISE–778234), the National Natural Science Foundation of China (Joint Research Project 81471100), and the European Foundation of Biomedical Research FERB Onlus. J.D.S. and E.T. are funded by a grant from STIC-AmSud (project SILIDOC - 21-STIC-11), ECOS-Sud A20M02, and ECOS-Sud U20S01. J.D.S. and G.D. are supported by the ModelDXConsciousness in the framework of the FLAG-ERA JTC 2021—HBP—2021 programme. E.T. is supported by PICT-2019-02294 (Agencia I+D+i, Argentina) and ANID/FONDECYT Regular 1220995 (Chile). The content of the article is solely the responsibility of the authors and does not represent the official views of these institutions. Y.S.P. A.I. M.L.K. S.L. G.D. and E.T. designed the research. Y.S.P. and E.T. conducted the research. Y.S.P. G.D. and E.T. analyzed and interpreted the results. A.D. C.M. V.B. J.D.S. J.A. O.G. N.A. R.P. H.L. and E.T. curated the data. Y.S.P. and E.T. wrote the manuscript and made figures. Y.S.P. analyzed the data. Y.S.P. G.D. and E.T. created and published the code. G.D. and E.T. supervised the research. All authors provided analytic support. All authors edited the manuscript. The authors declare no competing interests. We support inclusive, diverse, and equitable conduct of research. Funding Information: The authors thank participants and their families for their invaluable time and commitment to our study. The authors thank the whole staff from the Radiodiagnostic and Nuclear Medicine departments, University Hospital of Liege, especially Roland Hustinx, Claire Bernard, Jean-Flory Tshibanda, and Nathalie Maquet. Y.S.P. is supported by the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant 896354 . E.T. is supported by PICT - 2019-02294 (Agencia I+D+i, Argentina) and ANID / FONDECYT Regular 1220995 (Chile). A.I. is supported by grants from Takeda CW2680521 ; CONICET ; FONCYT- PICT ( 2017-1818 , 2017-1820 ); ANID / FONDECYT Regular ( 1210195 , 1210176 , and 1220995 ); ANID / FONDAP ( 15150012 ); ANID / PIA / ANILLOS ACT210096 ; and the Multi-Partner Consortium to Expand Dementia Research in Latin America (ReDLat), funded by the National Institutes of Aging of the National Institutes of Health under award number R01AG057234 , an Alzheimer's Association grant ( SG-20-725707-ReDLat ), the Rainwater Foundation , and the Global Brain Health Institute (GBHI). R.P. is post-doctoral fellow, O.G. is research associate, and S.L. is research director at FRS-FNRS. The study was further supported by the University and University Hospital of Liège ; the Belgian National Funds for Scientific Research (FRS-FNRS); the European Union’s Horizon 2020 Framework Programme for Research and Innovation under the Specific Grant Agreement No. 945539 (Human Brain Project SGA3); the FNRS PDR project ( T.0134.21 ); the ERA-Net FLAG-ERA JTC2021 project ModelDXConsciousness (Human Brain Project Partnering Project); the fund Generet ; the King Baudouin Foundation ; the Télévie Foundation ; the European Space Agency (ESA); and the Belgian Federal Science Policy Office ( BELSPO ) in the framework of the PRODEX Programme, the Public Utility Foundation “ Université Européenne du Travail ,” “ Fondazione Europea Ricerca Biomedica ,” the Bial Foundation , the Mind Science Foundation , the European Commission , the Fondation Léon Fredericq , the Mind-Care foundation , the DOCMA project ( EU-H2020-MSCA–RISE–778234 ), the National Natural Science Foundation of China (Joint Research Project 81471100 ), and the European Foundation of Biomedical Research FERB Onlus. J.D.S. and E.T. are funded by a grant from STIC-AmSud (project SILIDOC - 21-STIC-11), ECOS-Sud A20M02, and ECOS-Sud U20S01. J.D.S. and G.D. are supported by the ModelDXConsciousness in the framework of the FLAG-ERA JTC 2021—HBP—2021 programme. E.T. is supported by PICT-2019-02294 (Agencia I+D+i, Argentina) and ANID/FONDECYT Regular 1220995 (Chile). The content of the article is solely the responsibility of the authors and does not represent the official views of these institutions. Publisher Copyright: © 2023 The Authors

PY - 2023/5/30

Y1 - 2023/5/30

N2 - Brain states are frequently represented using a unidimensional scale measuring the richness of subjective experience (level of consciousness). This description assumes a mapping between the high-dimensional space of whole-brain configurations and the trajectories of brain states associated with changes in consciousness, yet this mapping and its properties remain unclear. We combine whole-brain modeling, data augmentation, and deep learning for dimensionality reduction to determine a mapping representing states of consciousness in a low-dimensional space, where distances parallel similarities between states. An orderly trajectory from wakefulness to patients with brain injury is revealed in a latent space whose coordinates represent metrics related to functional modularity and structure-function coupling, increasing alongside loss of consciousness. Finally, we investigate the effects of model perturbations, providing geometrical interpretation for the stability and reversibility of states. We conclude that conscious awareness depends on functional patterns encoded as a low-dimensional trajectory within the vast space of brain configurations.

AB - Brain states are frequently represented using a unidimensional scale measuring the richness of subjective experience (level of consciousness). This description assumes a mapping between the high-dimensional space of whole-brain configurations and the trajectories of brain states associated with changes in consciousness, yet this mapping and its properties remain unclear. We combine whole-brain modeling, data augmentation, and deep learning for dimensionality reduction to determine a mapping representing states of consciousness in a low-dimensional space, where distances parallel similarities between states. An orderly trajectory from wakefulness to patients with brain injury is revealed in a latent space whose coordinates represent metrics related to functional modularity and structure-function coupling, increasing alongside loss of consciousness. Finally, we investigate the effects of model perturbations, providing geometrical interpretation for the stability and reversibility of states. We conclude that conscious awareness depends on functional patterns encoded as a low-dimensional trajectory within the vast space of brain configurations.

KW - CP: Neuroscience

KW - deep learning

KW - fMRI

KW - low-dimensional brain dynamics

KW - reduced consciousness

KW - variational autoencoders

KW - whole-brain modeling

UR - http://www.scopus.com/inward/record.url?scp=85159069581&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2023.112491

DO - 10.1016/j.celrep.2023.112491

M3 - Article

AN - SCOPUS:85159069581

SN - 2211-1247

VL - 42

JO - Cell Reports

JF - Cell Reports

IS - 5

M1 - 112491

ER -

Low-dimensional organization of global brain states of reduced consciousness

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