Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairments

Parkinson’s disease (PD) is a neurodegenerative disease which presents clinically with progressive impairments in motoric and cognitive functioning. Pathophysiologic mechanisms underlying these impairments are believed to be attributable to a breakdown in the spatiotemporal coordination of functiona...

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Main Authors: Aaron S. Kemp, A. Journey Eubank, Yahya Younus, James E. Galvin, Fred W. Prior, Linda J. Larson-Prior
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:NeuroImage: Clinical
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Online Access:http://www.sciencedirect.com/science/article/pii/S221315822500049X
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author Aaron S. Kemp
A. Journey Eubank
Yahya Younus
James E. Galvin
Fred W. Prior
Linda J. Larson-Prior
author_facet Aaron S. Kemp
A. Journey Eubank
Yahya Younus
James E. Galvin
Fred W. Prior
Linda J. Larson-Prior
author_sort Aaron S. Kemp
collection DOAJ
description Parkinson’s disease (PD) is a neurodegenerative disease which presents clinically with progressive impairments in motoric and cognitive functioning. Pathophysiologic mechanisms underlying these impairments are believed to be attributable to a breakdown in the spatiotemporal coordination of functional neural networks across multiple cortical and subcortical regions. The current investigation used resting state, functional magnetic resonance imaging (rs-fMRI) to determine whether the temporal characteristics or sequential patterning of dynamic functional network connectivity (dFNC) states could accurately distinguish among people with PD who had normal cognition (PD-NC, n = 18), those with PD who had mild cognitive impairment (PD-MCI, n = 15), and older-aged healthy control (HC, n = 22) individuals. Results indicated that the proportion of time during the rs-fMRI scan that was spent in each of three identified dFNC states (dwell time) differed among these three groups. Individuals in the PD-MCI group spent significantly more time in a dFNC state characterized by low functional network connectivity, relative to participants in both the PD-NC (p = 0.0226) and HC (p = 0.0027) cohorts and tend to spend less time in a state characterized by anti-correlated thalamo-cortical connectivity, relative to both the PD-NC (p = 0.016) and HC (p = 0.0562) groups. A machine-learning method using sequential pattern mining was also found to distinguish among the groups with moderate accuracies ranging from 0.53 to 0.80, revealing distinct sequential patterns in the temporal ordering of dFNC states. These findings underscore the potential of dFNC and sequential pattern mining as relevant methods for further exploration of the pathophysiologic underpinnings of cognitive impairment among people living with PD.
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spelling doaj-art-0b8b4cb40a7c4baabec778e3d671b59f2025-08-20T03:26:35ZengElsevierNeuroImage: Clinical2213-15822025-01-014610377910.1016/j.nicl.2025.103779Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairmentsAaron S. Kemp0A. Journey Eubank1Yahya Younus2James E. Galvin3Fred W. Prior4Linda J. Larson-Prior5Department of Biomedical Informatics, 4301 W. Markham St., Little Rock, AR 72205, United States; Arkansas Children’s Research Institute, 13 Children’s Way, Little Rock, AR 72202, United States; Corresponding author at: Department of Biomedical Informatics, 4301 W. Markham St., Little Rock, AR 72205, United States.Department of Biomedical Informatics, 4301 W. Markham St., Little Rock, AR 72205, United StatesLittle Rock Central High School, 1500 S. Little Rock Nine Way, Little Rock, AR 72202, United StatesDepartment of Neurology, University of Miami, Miller School of Medicine, Comprehensive Center for Brain Health, 7700 W Camino Real, Suite 200, Boca Raton, FL 33433, United StatesDepartment of Biomedical Informatics, 4301 W. Markham St., Little Rock, AR 72205, United States; Arkansas Children’s Research Institute, 13 Children’s Way, Little Rock, AR 72202, United StatesDepartment of Biomedical Informatics, 4301 W. Markham St., Little Rock, AR 72205, United States; Department of Neurology, 4301 W. Markham St., Little Rock, AR 72205, United States; Department of Neurobiology & Developmental Sciences, 4301 W. Markham St., Little Rock, AR 72205, United States; Department of Pediatrics, at the University of Arkansas for Medical Sciences (UAMS), 4301 W. Markham St., Little Rock, AR 72205, United States; Arkansas Children’s Research Institute, 13 Children’s Way, Little Rock, AR 72202, United StatesParkinson’s disease (PD) is a neurodegenerative disease which presents clinically with progressive impairments in motoric and cognitive functioning. Pathophysiologic mechanisms underlying these impairments are believed to be attributable to a breakdown in the spatiotemporal coordination of functional neural networks across multiple cortical and subcortical regions. The current investigation used resting state, functional magnetic resonance imaging (rs-fMRI) to determine whether the temporal characteristics or sequential patterning of dynamic functional network connectivity (dFNC) states could accurately distinguish among people with PD who had normal cognition (PD-NC, n = 18), those with PD who had mild cognitive impairment (PD-MCI, n = 15), and older-aged healthy control (HC, n = 22) individuals. Results indicated that the proportion of time during the rs-fMRI scan that was spent in each of three identified dFNC states (dwell time) differed among these three groups. Individuals in the PD-MCI group spent significantly more time in a dFNC state characterized by low functional network connectivity, relative to participants in both the PD-NC (p = 0.0226) and HC (p = 0.0027) cohorts and tend to spend less time in a state characterized by anti-correlated thalamo-cortical connectivity, relative to both the PD-NC (p = 0.016) and HC (p = 0.0562) groups. A machine-learning method using sequential pattern mining was also found to distinguish among the groups with moderate accuracies ranging from 0.53 to 0.80, revealing distinct sequential patterns in the temporal ordering of dFNC states. These findings underscore the potential of dFNC and sequential pattern mining as relevant methods for further exploration of the pathophysiologic underpinnings of cognitive impairment among people living with PD.http://www.sciencedirect.com/science/article/pii/S221315822500049XBrain statesDynamic functional network connectivity (dFNC)Functional magnetic resonance imaging (fMRI)Machine learningMild cognitive impairment (MCI)Parkinson’s disease
spellingShingle Aaron S. Kemp
A. Journey Eubank
Yahya Younus
James E. Galvin
Fred W. Prior
Linda J. Larson-Prior
Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairments
NeuroImage: Clinical
Brain states
Dynamic functional network connectivity (dFNC)
Functional magnetic resonance imaging (fMRI)
Machine learning
Mild cognitive impairment (MCI)
Parkinson’s disease
title Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairments
title_full Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairments
title_fullStr Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairments
title_full_unstemmed Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairments
title_short Sequential patterning of dynamic brain states distinguish Parkinson’s disease patients with mild cognitive impairments
title_sort sequential patterning of dynamic brain states distinguish parkinson s disease patients with mild cognitive impairments
topic Brain states
Dynamic functional network connectivity (dFNC)
Functional magnetic resonance imaging (fMRI)
Machine learning
Mild cognitive impairment (MCI)
Parkinson’s disease
url http://www.sciencedirect.com/science/article/pii/S221315822500049X
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