The arrow of time in Parkinson’s disease
Background: Parkinson’s disease (PD) is a system-level disorder that implicates brain network dynamics across multiple scales. Detecting the ‘arrow of time’, or temporal reversibility of the brain’s information processing flow enables quantification of equilibrium in the brain and inferences on the...
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| Format: | Article |
| Language: | English |
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Elsevier
2025-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158225001044 |
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| author | Fatemeh Sadeghi Elvira del Agua Banyeres Alessandra Pizzuti Abdullah Okar Kai Grimm Christian Gerloff Morten L. Kringelbach Rainer Goebel Simone Zittel Gustavo Deco |
| author_facet | Fatemeh Sadeghi Elvira del Agua Banyeres Alessandra Pizzuti Abdullah Okar Kai Grimm Christian Gerloff Morten L. Kringelbach Rainer Goebel Simone Zittel Gustavo Deco |
| author_sort | Fatemeh Sadeghi |
| collection | DOAJ |
| description | Background: Parkinson’s disease (PD) is a system-level disorder that implicates brain network dynamics across multiple scales. Detecting the ‘arrow of time’, or temporal reversibility of the brain’s information processing flow enables quantification of equilibrium in the brain and inferences on the hierarchical organization. Therefore we aimed to explore disturbances in resting-state equilibrium levels as well as changes in the hierarchical organization due to PD. Methods: Structural and functional MRI of 29 PD patients and 19 healthy controls were acquired and analyzed. Empirical non-reversibility was computed as the distance between time-shifted forward- and artificially-reversed time series. Levels of equilibrium were subsequently assessed globally and within two cortico-subcortical motor networks implicated in PD. Moreover, whole-brain generative computational models consisting of 1051 Hopf oscillators were constructed to evaluate effective connectivities and alterations of the functional hierarchical organization. Results: We found that PD is characterized by disrupted equilibrium regimes, marked by distinct effective connectivity patterns, particularly within the motor networks. Additionally, we observed a flatter hierarchical organization in PD, with the cerebellum and thalamus exerting increased influence. Conclusion: The arrow of time methodology effectively identifies distinct and informative characteristics of PD. Our analyses suggest that PD shifts the brain towards less efficient, non-equilibrium dynamics that impair intrinsic flexibility and disrupt motor coordination. Thus, these findings not only provide insight into widespread system alterations in PD that could serve as potential biomarkers, but also lay the groundwork for next-generation stimulation techniques aimed at restoring balance in the Parkinsonian brain. |
| format | Article |
| id | doaj-art-7c2ca359fef44c9c9bf79e81835829e1 |
| institution | Kabale University |
| issn | 2213-1582 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj-art-7c2ca359fef44c9c9bf79e81835829e12025-08-20T03:30:49ZengElsevierNeuroImage: Clinical2213-15822025-01-014710383410.1016/j.nicl.2025.103834The arrow of time in Parkinson’s diseaseFatemeh Sadeghi0Elvira del Agua Banyeres1Alessandra Pizzuti2Abdullah Okar3Kai Grimm4Christian Gerloff5Morten L. Kringelbach6Rainer Goebel7Simone Zittel8Gustavo Deco9Department of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyCenter for Brain and Cognition, Computational Neuroscience Group, Universitat Pompeu Fabra, 08005 Barcelona, SpainDepartment of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6211 LK Maastricht, the Netherlands; Brain Innovation B.V., 6229 EV Maastricht, the NetherlandsDepartment of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyDepartment of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyCentre for Eudaimonia and Human Flourishing, Linacre College, University of Oxford, Oxford OX1 3JA, UK; Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, 4710-057 Braga, Portugal; Center for Music in the Brain, Department of Clinical Medicine, Aarhus University, 8000 Aarhus, Denmark; Department of Psychiatry, University of Oxford, Oxford OX3 7JX, UKDepartment of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, 6211 LK Maastricht, the Netherlands; Brain Innovation B.V., 6229 EV Maastricht, the NetherlandsDepartment of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, GermanyCenter for Brain and Cognition, Computational Neuroscience Group, Universitat Pompeu Fabra, 08005 Barcelona, Spain; Department of Information and Communication Technologies, Universitat Pompeu Fabra, 08018 Barcelona, Spain; Institució Catalana de la Recerca i Estudis Avancats (ICREA), 08010 Barcelona, Spain; Corresponding author at: Center for Brain and Cognition, Computational Neuroscience Group, Universitat Pompeu Fabra, 08005 Barcelona, Spain.Background: Parkinson’s disease (PD) is a system-level disorder that implicates brain network dynamics across multiple scales. Detecting the ‘arrow of time’, or temporal reversibility of the brain’s information processing flow enables quantification of equilibrium in the brain and inferences on the hierarchical organization. Therefore we aimed to explore disturbances in resting-state equilibrium levels as well as changes in the hierarchical organization due to PD. Methods: Structural and functional MRI of 29 PD patients and 19 healthy controls were acquired and analyzed. Empirical non-reversibility was computed as the distance between time-shifted forward- and artificially-reversed time series. Levels of equilibrium were subsequently assessed globally and within two cortico-subcortical motor networks implicated in PD. Moreover, whole-brain generative computational models consisting of 1051 Hopf oscillators were constructed to evaluate effective connectivities and alterations of the functional hierarchical organization. Results: We found that PD is characterized by disrupted equilibrium regimes, marked by distinct effective connectivity patterns, particularly within the motor networks. Additionally, we observed a flatter hierarchical organization in PD, with the cerebellum and thalamus exerting increased influence. Conclusion: The arrow of time methodology effectively identifies distinct and informative characteristics of PD. Our analyses suggest that PD shifts the brain towards less efficient, non-equilibrium dynamics that impair intrinsic flexibility and disrupt motor coordination. Thus, these findings not only provide insight into widespread system alterations in PD that could serve as potential biomarkers, but also lay the groundwork for next-generation stimulation techniques aimed at restoring balance in the Parkinsonian brain.http://www.sciencedirect.com/science/article/pii/S2213158225001044Arrow of timeBrain dynamicsEquilibriumHierarchical organizationNon-reversibilityParkinson’s disease |
| spellingShingle | Fatemeh Sadeghi Elvira del Agua Banyeres Alessandra Pizzuti Abdullah Okar Kai Grimm Christian Gerloff Morten L. Kringelbach Rainer Goebel Simone Zittel Gustavo Deco The arrow of time in Parkinson’s disease NeuroImage: Clinical Arrow of time Brain dynamics Equilibrium Hierarchical organization Non-reversibility Parkinson’s disease |
| title | The arrow of time in Parkinson’s disease |
| title_full | The arrow of time in Parkinson’s disease |
| title_fullStr | The arrow of time in Parkinson’s disease |
| title_full_unstemmed | The arrow of time in Parkinson’s disease |
| title_short | The arrow of time in Parkinson’s disease |
| title_sort | arrow of time in parkinson s disease |
| topic | Arrow of time Brain dynamics Equilibrium Hierarchical organization Non-reversibility Parkinson’s disease |
| url | http://www.sciencedirect.com/science/article/pii/S2213158225001044 |
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