LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics

A topic of growing interest in computational neuroscience is the discovery of fundamental principles underlying global dynamics and the self-organization of the brain. In particular, the notion that the brain operates near criticality has gained considerable support, and recent work has shown that t...

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Authors: Ruffini, Giulio, Damiani, Giada, Lozano-Soldevilla, Diego, Deco, Nikolas, Rosas, Fernando E., Kiani, Narsis A., Ponce Álvarez, Adrián Fernando|||0000-0003-1446-7392, Kringelbach, Morten L., Carhart-Harris, Robin, Deco, Gustavo
Format: article
Publication Date:2023
Country:España
Institution:Universitat Politècnica de Catalunya (UPC)
Repository:UPCommons. Portal del coneixement obert de la UPC
Language:English
OAI Identifier:oai:upcommons.upc.edu:2117/401591
Online Access:https://hdl.handle.net/2117/401591
https://dx.doi.org/10.1371/journal.pcbi.1010811
Access Level:Open access
Keyword:Neurology
Brain -- Research
Neurologia
Cervell -- Investigació
Classificació AMS::92 Biology and other natural sciences::92C Physiological, cellular and medical topics
Àrees temàtiques de la UPC::Ciències de la salut::Medicina::Neurologia
Àrees temàtiques de la UPC::Enginyeria biomèdica
id ES_ef4cc9bbba7fe94e1668aa4c94ba65db
oai_identifier_str oai:upcommons.upc.edu:2117/401591
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
title LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
spellingShingle LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
Ruffini, Giulio
Neurology
Brain -- Research
Neurologia
Cervell -- Investigació
Classificació AMS::92 Biology and other natural sciences::92C Physiological, cellular and medical topics
Àrees temàtiques de la UPC::Ciències de la salut::Medicina::Neurologia
Àrees temàtiques de la UPC::Enginyeria biomèdica
title_short LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
title_full LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
title_fullStr LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
title_full_unstemmed LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
title_sort LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics
dc.creator.none.fl_str_mv Ruffini, Giulio
Damiani, Giada
Lozano-Soldevilla, Diego
Deco, Nikolas
Rosas, Fernando E.
Kiani, Narsis A.
Ponce Álvarez, Adrián Fernando|||0000-0003-1446-7392
Kringelbach, Morten L.
Carhart-Harris, Robin
Deco, Gustavo
author Ruffini, Giulio
author_facet Ruffini, Giulio
Damiani, Giada
Lozano-Soldevilla, Diego
Deco, Nikolas
Rosas, Fernando E.
Kiani, Narsis A.
Ponce Álvarez, Adrián Fernando|||0000-0003-1446-7392
Kringelbach, Morten L.
Carhart-Harris, Robin
Deco, Gustavo
author_role author
author2 Damiani, Giada
Lozano-Soldevilla, Diego
Deco, Nikolas
Rosas, Fernando E.
Kiani, Narsis A.
Ponce Álvarez, Adrián Fernando|||0000-0003-1446-7392
Kringelbach, Morten L.
Carhart-Harris, Robin
Deco, Gustavo
author2_role author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Neurology
Brain -- Research
Neurologia
Cervell -- Investigació
Classificació AMS::92 Biology and other natural sciences::92C Physiological, cellular and medical topics
Àrees temàtiques de la UPC::Ciències de la salut::Medicina::Neurologia
Àrees temàtiques de la UPC::Enginyeria biomèdica
topic Neurology
Brain -- Research
Neurologia
Cervell -- Investigació
Classificació AMS::92 Biology and other natural sciences::92C Physiological, cellular and medical topics
Àrees temàtiques de la UPC::Ciències de la salut::Medicina::Neurologia
Àrees temàtiques de la UPC::Enginyeria biomèdica
description A topic of growing interest in computational neuroscience is the discovery of fundamental principles underlying global dynamics and the self-organization of the brain. In particular, the notion that the brain operates near criticality has gained considerable support, and recent work has shown that the dynamics of different brain states may be modeled by pairwise maximum entropy Ising models at various distances from a phase transition, i.e., from criticality. Here we aim to characterize two brain states (psychedelics-induced and placebo) as captured by functional magnetic resonance imaging (fMRI), with features derived from the Ising spin model formalism (system temperature, critical point, susceptibility) and from algorithmic complexity. We hypothesized, along the lines of the entropic brain hypothesis, that psychedelics drive brain dynamics into a more disordered state at a higher Ising temperature and increased complexity. We analyze resting state blood-oxygen-level-dependent (BOLD) fMRI data collected in an earlier study from fifteen subjects in a control condition (placebo) and during ingestion of lysergic acid diethylamide (LSD). Working with the automated anatomical labeling (AAL) brain parcellation, we first create “archetype” Ising models representative of the entire dataset (global) and of the data in each condition. Remarkably, we find that such archetypes exhibit a strong correlation with an average structural connectome template obtained from dMRI (r = 0.6). We compare the archetypes from the two conditions and find that the Ising connectivity in the LSD condition is lower than in the placebo one, especially in homotopic links (interhemispheric connectivity), reflecting a significant decrease of homotopic functional connectivity in the LSD condition. The global archetype is then personalized for each individual and condition by adjusting the system temperature. The resulting temperatures are all near but above the critical point of the model in the paramagnetic (disordered) phase. The individualized Ising temperatures are higher in the LSD condition than in the placebo condition (p = 9 × 10-5). Next, we estimate the Lempel-Ziv-Welch (LZW) complexity of the binarized BOLD data and the synthetic data generated with the individualized model using the Metropolis algorithm for each participant and condition. The LZW complexity computed from experimental data reveals a weak statistical relationship with condition (p = 0.04 one-tailed Wilcoxon test) and none with Ising temperature (r(13) = 0.13, p = 0.65), presumably because of the limited length of the BOLD time series. Similarly, we explore complexity using the block decomposition method (BDM), a more advanced method for estimating algorithmic complexity. The BDM complexity of the experimental data displays a significant correlation with Ising temperature (r(13) = 0.56, p = 0.03) and a weak but significant correlation with condition (p = 0.04, one-tailed Wilcoxon test). This study suggests that the effects of LSD increase the complexity of brain dynamics by loosening interhemispheric connectivity—especially homotopic links. In agreement with earlier work using the Ising formalism with BOLD data, we find the brain state in the placebo condition is already above the critical point, with LSD resulting in a shift further away from criticality into a more disordered state.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023-02-03
2024
2024-02-09
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv https://hdl.handle.net/2117/401591
https://dx.doi.org/10.1371/journal.pcbi.1010811
url https://hdl.handle.net/2117/401591
https://dx.doi.org/10.1371/journal.pcbi.1010811
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
Attribution-NonCommercial-NoDerivatives 4.0 International
http://creativecommons.org/licenses/by-nc-nd/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Public Library of Science (PLOS)
publisher.none.fl_str_mv Public Library of Science (PLOS)
dc.source.none.fl_str_mv reponame:UPCommons. Portal del coneixement obert de la UPC
instname:Universitat Politècnica de Catalunya (UPC)
instname_str Universitat Politècnica de Catalunya (UPC)
reponame_str UPCommons. Portal del coneixement obert de la UPC
collection UPCommons. Portal del coneixement obert de la UPC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamicsRuffini, GiulioDamiani, GiadaLozano-Soldevilla, DiegoDeco, NikolasRosas, Fernando E.Kiani, Narsis A.Ponce Álvarez, Adrián Fernando|||0000-0003-1446-7392Kringelbach, Morten L.Carhart-Harris, RobinDeco, GustavoNeurologyBrain -- ResearchNeurologiaCervell -- InvestigacióClassificació AMS::92 Biology and other natural sciences::92C Physiological, cellular and medical topicsÀrees temàtiques de la UPC::Ciències de la salut::Medicina::NeurologiaÀrees temàtiques de la UPC::Enginyeria biomèdicaA topic of growing interest in computational neuroscience is the discovery of fundamental principles underlying global dynamics and the self-organization of the brain. In particular, the notion that the brain operates near criticality has gained considerable support, and recent work has shown that the dynamics of different brain states may be modeled by pairwise maximum entropy Ising models at various distances from a phase transition, i.e., from criticality. Here we aim to characterize two brain states (psychedelics-induced and placebo) as captured by functional magnetic resonance imaging (fMRI), with features derived from the Ising spin model formalism (system temperature, critical point, susceptibility) and from algorithmic complexity. We hypothesized, along the lines of the entropic brain hypothesis, that psychedelics drive brain dynamics into a more disordered state at a higher Ising temperature and increased complexity. We analyze resting state blood-oxygen-level-dependent (BOLD) fMRI data collected in an earlier study from fifteen subjects in a control condition (placebo) and during ingestion of lysergic acid diethylamide (LSD). Working with the automated anatomical labeling (AAL) brain parcellation, we first create “archetype” Ising models representative of the entire dataset (global) and of the data in each condition. Remarkably, we find that such archetypes exhibit a strong correlation with an average structural connectome template obtained from dMRI (r = 0.6). We compare the archetypes from the two conditions and find that the Ising connectivity in the LSD condition is lower than in the placebo one, especially in homotopic links (interhemispheric connectivity), reflecting a significant decrease of homotopic functional connectivity in the LSD condition. The global archetype is then personalized for each individual and condition by adjusting the system temperature. The resulting temperatures are all near but above the critical point of the model in the paramagnetic (disordered) phase. The individualized Ising temperatures are higher in the LSD condition than in the placebo condition (p = 9 × 10-5). Next, we estimate the Lempel-Ziv-Welch (LZW) complexity of the binarized BOLD data and the synthetic data generated with the individualized model using the Metropolis algorithm for each participant and condition. The LZW complexity computed from experimental data reveals a weak statistical relationship with condition (p = 0.04 one-tailed Wilcoxon test) and none with Ising temperature (r(13) = 0.13, p = 0.65), presumably because of the limited length of the BOLD time series. Similarly, we explore complexity using the block decomposition method (BDM), a more advanced method for estimating algorithmic complexity. The BDM complexity of the experimental data displays a significant correlation with Ising temperature (r(13) = 0.56, p = 0.03) and a weak but significant correlation with condition (p = 0.04, one-tailed Wilcoxon test). This study suggests that the effects of LSD increase the complexity of brain dynamics by loosening interhemispheric connectivity—especially homotopic links. In agreement with earlier work using the Ising formalism with BOLD data, we find the brain state in the placebo condition is already above the critical point, with LSD resulting in a shift further away from criticality into a more disordered state.Funding: GR, GiD, DL-S, ND have received funding from the European Research Council (ERC Synergy Galvani) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No 855109). GR, GD, GiD, DL-S and ND have received funding from European Union’s Horizon 2020 research and innovation programme under grant agreement No 101017716 (Neurotwin). FER is supported by the Ad Astra Chandaria foundation. NAK has received funding from the European Union under the Horizon 2020 programme (MultipleMS grant agreement 733161 and DECISION Grant agreement 847949). AP-A was supported by the Human Brain Project SGA3 (945539) and the Ramo´n y Cajal fellowship (RYC2020-029117-I). RC-H is supported by the Ralph Metzner Distinguished Professorship endowment. GD has received funding from the Spanish national research project (ref. AEIPID2019-105772GB-I00/AEI/10.13039/ 501100011033) funded by the Spanish Ministry of Science, Innovation and Universities (MCIU), State Research Agency (AEI). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Peer ReviewedPublic Library of Science (PLOS)20232023-02-0320242024-02-09journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/2117/401591https://dx.doi.org/10.1371/journal.pcbi.1010811reponame:UPCommons. Portal del coneixement obert de la UPCinstname:Universitat Politècnica de Catalunya (UPC)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Attribution-NonCommercial-NoDerivatives 4.0 Internationalhttp://creativecommons.org/licenses/by-nc-nd/4.0/info:eu-repo/semantics/openAccessoai:upcommons.upc.edu:2117/4015912026-05-27T15:37:01Z
score 15.300719

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