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

Ruffini, G., Damiani, G., Lozano-Soldevilla, D., Deco, N., Rosas, F. E., Kiani, N. A., et al. (2023). LSD-induced increase of Ising temperature and algorithmic complexity of brain dynamics. PLoS Computational Biology, 19(2): e1010811. doi:10.1371/journal.pcbi.1010811.

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 Urheber:
Ruffini, Giulio1, 2, 3, Autor
Damiani, Giada1, Autor
Lozano-Soldevilla, Diego1, Autor
Deco, Nikolas1, Autor
Rosas, Fernando E.4, 5, 6, 7, Autor
Kiani, Narsis A.8, 9, Autor
Ponce-Alvarez, Adrián10, Autor
Kringelbach, Morten L.7, 11, 12, Autor
Carhart-Harris, Robin5, 13, Autor
Deco, Gustavo14, 15, 16, Autor           
Affiliations:
1Neuroelectrics Barcelona, Spain, ou_persistent22              
2Starlab Barcelona, Spain, ou_persistent22              
3Haskins Laboratories, New Haven, CT, USA, ou_persistent22              
4Department of Informatics, University of Sussex, Brighton, United Kingdom, ou_persistent22              
5Psychedelic Research Group, Division of Brain Sciences, Faculty of Medicine, Imperial College London, United Kingdom, ou_persistent22              
6Centre for Complexity Science, Imperial College London, United Kingdom, ou_persistent22              
7Centre for Eudaimonia and Human Flourishing, University of Oxford, United Kingdom, ou_persistent22              
8Algorithmic Dynamics Lab, Center of Molecular Medicine, Karolinska Institute, Stockholm, Sweden, ou_persistent22              
9Department of Oncology-Pathology, Karolinska Institute, Stockholm, Sweden, ou_persistent22              
10Computational Neuroscience Group, Department of Information and Communication Technologies, Center for Brain and Cognition, University Pompeu Fabra, Barcelona, Spain, ou_persistent22              
11Department of Psychiatry, University of Oxford, United Kingdom, ou_persistent22              
12Center for Music in the Brain, Aarhus University, Denmark, ou_persistent22              
13Neuroscape Psychedelics Division, University of California, San Francisco, CA, USA, ou_persistent22              
14Catalan Institution for Research and Advanced Studies (ICREA), University Pompeu Fabra, Barcelona, Spain, ou_persistent22              
15Department Neuropsychology, MPI for Human Cognitive and Brain Sciences, Max Planck Society, ou_634551              
16School of Psychological Sciences, Monash University, Melbourne, Australia, ou_persistent22              

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 Zusammenfassung: 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 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 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.

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Sprache(n): eng - English
 Datum: 2022-09-012022-12-112023-02-032023-02-03
 Publikationsstatus: Erschienen
 Seiten: -
 Ort, Verlag, Ausgabe: -
 Inhaltsverzeichnis: -
 Art der Begutachtung: -
 Identifikatoren: DOI: 10.1371/journal.pcbi.1010811
Anderer: eCollection 2023
PMID: 36735751
 Art des Abschluß: -

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Projektname : -
Grant ID : 855109; 101017716; 733161; 847949
Förderprogramm : Horizon 2020
Förderorganisation : European Union
Projektname : -
Grant ID : 945539
Förderprogramm : -
Förderorganisation : Human Brain Project (HBP)
Projektname : -
Grant ID : RYC2020-029117-I
Förderprogramm : -
Förderorganisation : Ramón y Cajal fellowship

Quelle 1

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Titel: PLoS Computational Biology
Genre der Quelle: Zeitschrift
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Affiliations:
Ort, Verlag, Ausgabe: San Francisco, CA : Public Library of Science
Seiten: - Band / Heft: 19 (2) Artikelnummer: e1010811 Start- / Endseite: - Identifikator: ISSN: 1553-734X
CoNE: https://pure.mpg.de/cone/journals/resource/1000000000017180_1