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...

Full description

Saved in:
Bibliographic Details
Main Authors: Fatemeh Sadeghi, Elvira del Agua Banyeres, Alessandra Pizzuti, Abdullah Okar, Kai Grimm, Christian Gerloff, Morten L. Kringelbach, Rainer Goebel, Simone Zittel, Gustavo Deco
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158225001044
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849423020454576128
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
work_keys_str_mv AT fatemehsadeghi thearrowoftimeinparkinsonsdisease
AT elviradelaguabanyeres thearrowoftimeinparkinsonsdisease
AT alessandrapizzuti thearrowoftimeinparkinsonsdisease
AT abdullahokar thearrowoftimeinparkinsonsdisease
AT kaigrimm thearrowoftimeinparkinsonsdisease
AT christiangerloff thearrowoftimeinparkinsonsdisease
AT mortenlkringelbach thearrowoftimeinparkinsonsdisease
AT rainergoebel thearrowoftimeinparkinsonsdisease
AT simonezittel thearrowoftimeinparkinsonsdisease
AT gustavodeco thearrowoftimeinparkinsonsdisease
AT fatemehsadeghi arrowoftimeinparkinsonsdisease
AT elviradelaguabanyeres arrowoftimeinparkinsonsdisease
AT alessandrapizzuti arrowoftimeinparkinsonsdisease
AT abdullahokar arrowoftimeinparkinsonsdisease
AT kaigrimm arrowoftimeinparkinsonsdisease
AT christiangerloff arrowoftimeinparkinsonsdisease
AT mortenlkringelbach arrowoftimeinparkinsonsdisease
AT rainergoebel arrowoftimeinparkinsonsdisease
AT simonezittel arrowoftimeinparkinsonsdisease
AT gustavodeco arrowoftimeinparkinsonsdisease