Exploring dynamical whole-brain models in high-dimensional parameter spaces
Personalized modeling of the resting-state brain activity implies the usage of dynamical whole-brain models with high-dimensional model parameter spaces. However, the practical benefits and mathematical challenges originating from such approaches have not been thoroughly documented, leaving the ques...
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Published in | PloS one Vol. 20; no. 5; p. e0322983 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
United States
Public Library of Science
12.05.2025
Public Library of Science (PLoS) |
Subjects | |
Online Access | Get full text |
ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/journal.pone.0322983 |
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Abstract | Personalized modeling of the resting-state brain activity implies the usage of dynamical whole-brain models with high-dimensional model parameter spaces. However, the practical benefits and mathematical challenges originating from such approaches have not been thoroughly documented, leaving the question of the value and utility of high-dimensional approaches unanswered. Studying a whole-brain model of coupled phase oscillators, we proceeded from low-dimensional scenarios featuring 2–3 global model parameters only to high-dimensional cases, where we additionally equipped every brain region with a specific local model parameter. To enable the parameter optimizations for the high-dimensional model fitting to empirical data, we applied two dedicated mathematical optimization algorithms (Bayesian Optimization, Covariance Matrix Adaptation Evolution Strategy). We thereby optimized up to 103 parameters simultaneously with the aim to maximize the correlation between simulated and empirical functional connectivity separately for 272 subjects. The obtained model parameters demonstrated increased variability within subjects and reduced reliability across repeated optimization runs in high-dimensional spaces. Nevertheless, the quality of the model validation (goodness-of-fit, GoF) improved considerably and remained very stable and reliable together with the simulated functional connectivity. Applying the modeling results to phenotypical data, we found significantly higher prediction accuracies for sex classification when the GoF or coupling parameter values optimized in the high-dimensional spaces were considered as features. Our results elucidate the model fitting in high-dimensional parameter spaces and can contribute to an improved dynamical brain modeling as well as its application to the frameworks of inter-individual variability and brain-behavior relationships. |
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AbstractList | Personalized modeling of the resting-state brain activity implies the usage of dynamical whole-brain models with high-dimensional model parameter spaces. However, the practical benefits and mathematical challenges originating from such approaches have not been thoroughly documented, leaving the question of the value and utility of high-dimensional approaches unanswered. Studying a whole-brain model of coupled phase oscillators, we proceeded from low-dimensional scenarios featuring 2–3 global model parameters only to high-dimensional cases, where we additionally equipped every brain region with a specific local model parameter. To enable the parameter optimizations for the high-dimensional model fitting to empirical data, we applied two dedicated mathematical optimization algorithms (Bayesian Optimization, Covariance Matrix Adaptation Evolution Strategy). We thereby optimized up to 103 parameters simultaneously with the aim to maximize the correlation between simulated and empirical functional connectivity separately for 272 subjects. The obtained model parameters demonstrated increased variability within subjects and reduced reliability across repeated optimization runs in high-dimensional spaces. Nevertheless, the quality of the model validation (goodness-of-fit, GoF) improved considerably and remained very stable and reliable together with the simulated functional connectivity. Applying the modeling results to phenotypical data, we found significantly higher prediction accuracies for sex classification when the GoF or coupling parameter values optimized in the high-dimensional spaces were considered as features. Our results elucidate the model fitting in high-dimensional parameter spaces and can contribute to an improved dynamical brain modeling as well as its application to the frameworks of inter-individual variability and brain-behavior relationships. Personalized modeling of the resting-state brain activity implies the usage of dynamical whole-brain models with high-dimensional model parameter spaces. However, the practical benefits and mathematical challenges originating from such approaches have not been thoroughly documented, leaving the question of the value and utility of high-dimensional approaches unanswered. Studying a whole-brain model of coupled phase oscillators, we proceeded from low-dimensional scenarios featuring 2-3 global model parameters only to high-dimensional cases, where we additionally equipped every brain region with a specific local model parameter. To enable the parameter optimizations for the high-dimensional model fitting to empirical data, we applied two dedicated mathematical optimization algorithms (Bayesian Optimization, Covariance Matrix Adaptation Evolution Strategy). We thereby optimized up to 103 parameters simultaneously with the aim to maximize the correlation between simulated and empirical functional connectivity separately for 272 subjects. The obtained model parameters demonstrated increased variability within subjects and reduced reliability across repeated optimization runs in high-dimensional spaces. Nevertheless, the quality of the model validation (goodness-of-fit, GoF) improved considerably and remained very stable and reliable together with the simulated functional connectivity. Applying the modeling results to phenotypical data, we found significantly higher prediction accuracies for sex classification when the GoF or coupling parameter values optimized in the high-dimensional spaces were considered as features. Our results elucidate the model fitting in high-dimensional parameter spaces and can contribute to an improved dynamical brain modeling as well as its application to the frameworks of inter-individual variability and brain-behavior relationships.Personalized modeling of the resting-state brain activity implies the usage of dynamical whole-brain models with high-dimensional model parameter spaces. However, the practical benefits and mathematical challenges originating from such approaches have not been thoroughly documented, leaving the question of the value and utility of high-dimensional approaches unanswered. Studying a whole-brain model of coupled phase oscillators, we proceeded from low-dimensional scenarios featuring 2-3 global model parameters only to high-dimensional cases, where we additionally equipped every brain region with a specific local model parameter. To enable the parameter optimizations for the high-dimensional model fitting to empirical data, we applied two dedicated mathematical optimization algorithms (Bayesian Optimization, Covariance Matrix Adaptation Evolution Strategy). We thereby optimized up to 103 parameters simultaneously with the aim to maximize the correlation between simulated and empirical functional connectivity separately for 272 subjects. The obtained model parameters demonstrated increased variability within subjects and reduced reliability across repeated optimization runs in high-dimensional spaces. Nevertheless, the quality of the model validation (goodness-of-fit, GoF) improved considerably and remained very stable and reliable together with the simulated functional connectivity. Applying the modeling results to phenotypical data, we found significantly higher prediction accuracies for sex classification when the GoF or coupling parameter values optimized in the high-dimensional spaces were considered as features. Our results elucidate the model fitting in high-dimensional parameter spaces and can contribute to an improved dynamical brain modeling as well as its application to the frameworks of inter-individual variability and brain-behavior relationships. |
Audience | Academic |
Author | Popovych, Oleksandr V. Wischnewski, Kevin J. Jarre, Florian Eickhoff, Simon B. |
AuthorAffiliation | 1 Institute of Neuroscience and Medicine – Brain and Behaviour (INM-7), Forschungszentrum Jülich, Germany 3 Institute of Mathematics, Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf, Germany 2 Institute of Systems Neuroscience, Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany Western University, CANADA |
AuthorAffiliation_xml | – name: 1 Institute of Neuroscience and Medicine – Brain and Behaviour (INM-7), Forschungszentrum Jülich, Germany – name: 3 Institute of Mathematics, Faculty of Mathematics and Natural Sciences, Heinrich Heine University Düsseldorf, Germany – name: Western University, CANADA – name: 2 Institute of Systems Neuroscience, Medical Faculty and University Hospital Düsseldorf, Heinrich Heine University Düsseldorf, Germany |
Author_xml | – sequence: 1 givenname: Kevin J. orcidid: 0000-0003-3294-5706 surname: Wischnewski fullname: Wischnewski, Kevin J. – sequence: 2 givenname: Florian surname: Jarre fullname: Jarre, Florian – sequence: 3 givenname: Simon B. surname: Eickhoff fullname: Eickhoff, Simon B. – sequence: 4 givenname: Oleksandr V. orcidid: 0000-0001-9994-1764 surname: Popovych fullname: Popovych, Oleksandr V. |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/40354445$$D View this record in MEDLINE/PubMed |
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Copyright | Copyright: © 2025 Wischnewski et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. COPYRIGHT 2025 Public Library of Science 2025 Wischnewski et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2025 Wischnewski et al 2025 Wischnewski et al 2025 Wischnewski et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. |
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