Dynamics of Top‐Down Control and Motor Networks in Parkinson's Disease

Background Motor symptoms in Parkinson's disease (PD) patients might be related to high‐level task‐control deficits. We aimed at investigating the dynamics between sensorimotor network and top‐down control networks (frontal–parietal, cingulo‐opercular, and cerebellar) in PD and at determining t...

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Published in:Movement disorders Vol. 36; no. 4; pp. 916 - 926
Main Authors: Chen, Li, Bedard, Patrick, Hallett, Mark, Horovitz, Silvina G.
Format: Journal Article
Language:English
Published: Hoboken, USA John Wiley & Sons, Inc 01.04.2021
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ISSN:0885-3185, 1531-8257, 1531-8257
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Abstract Background Motor symptoms in Parkinson's disease (PD) patients might be related to high‐level task‐control deficits. We aimed at investigating the dynamics between sensorimotor network and top‐down control networks (frontal–parietal, cingulo‐opercular, and cerebellar) in PD and at determining the effects of levodopa on the dynamics of these networks. Methods We investigated dynamic functional connectivity (dFC), during resting state functional magnetic resonance imaging, between sensorimotor network and top‐down control networks in 36 PD patients (OFF medication, PD‐OFF) and 36 healthy volunteers. We further assessed the effect of medication on dFC in18 PD patients who were also scanned ON medication. Results The dFC analyses identified three discrete states: State I (35.68%) characterized by connections between the cerebellum and sensorimotor network, State II (34.17%) with connections between the sensorimotor and frontal–parietal network, and State III (30.15%) with connection between the sensorimotor and cingulo‐opercular network. PD patients have significantly fewer occurrences and overall spent less time (shorter dwell time) in State II compared to healthy controls. After levodopa intake, dwell time improved toward normal. The change in dwell time before and after taking levodopa was negatively related to the respective changes in Unified Parkinson's Disease Rating Scale, Part III. PD‐OFF showed significantly decreased connectivity between sensorimotor and control networks and increased connectivity within control networks. These changes were partially improved after levodopa intake. Conclusions Dopamine depletion in PD is associated with abnormalities in temporal and spatial properties between cognitive control and sensorimotor network, possibly contributing to clinical deficits. Levodopa partially restores the network function toward the values observed in healthy volunteers. © 2021 International Parkinson and Movement Disorder Society
AbstractList Motor symptoms in Parkinson's disease (PD) patients might be related to high-level task-control deficits. We aimed at investigating the dynamics between sensorimotor network and top-down control networks (frontal-parietal, cingulo-opercular, and cerebellar) in PD and at determining the effects of levodopa on the dynamics of these networks. We investigated dynamic functional connectivity (dFC), during resting state functional magnetic resonance imaging, between sensorimotor network and top-down control networks in 36 PD patients (OFF medication, PD-OFF) and 36 healthy volunteers. We further assessed the effect of medication on dFC in18 PD patients who were also scanned ON medication. The dFC analyses identified three discrete states: State I (35.68%) characterized by connections between the cerebellum and sensorimotor network, State II (34.17%) with connections between the sensorimotor and frontal-parietal network, and State III (30.15%) with connection between the sensorimotor and cingulo-opercular network. PD patients have significantly fewer occurrences and overall spent less time (shorter dwell time) in State II compared to healthy controls. After levodopa intake, dwell time improved toward normal. The change in dwell time before and after taking levodopa was negatively related to the respective changes in Unified Parkinson's Disease Rating Scale, Part III. PD-OFF showed significantly decreased connectivity between sensorimotor and control networks and increased connectivity within control networks. These changes were partially improved after levodopa intake. Dopamine depletion in PD is associated with abnormalities in temporal and spatial properties between cognitive control and sensorimotor network, possibly contributing to clinical deficits. Levodopa partially restores the network function toward the values observed in healthy volunteers. © 2021 International Parkinson and Movement Disorder Society.
Motor symptoms in Parkinson's disease (PD) patients might be related to high-level task-control deficits. We aimed at investigating the dynamics between sensorimotor network and top-down control networks (frontal-parietal, cingulo-opercular, and cerebellar) in PD and at determining the effects of levodopa on the dynamics of these networks.BACKGROUNDMotor symptoms in Parkinson's disease (PD) patients might be related to high-level task-control deficits. We aimed at investigating the dynamics between sensorimotor network and top-down control networks (frontal-parietal, cingulo-opercular, and cerebellar) in PD and at determining the effects of levodopa on the dynamics of these networks.We investigated dynamic functional connectivity (dFC), during resting state functional magnetic resonance imaging, between sensorimotor network and top-down control networks in 36 PD patients (OFF medication, PD-OFF) and 36 healthy volunteers. We further assessed the effect of medication on dFC in18 PD patients who were also scanned ON medication.METHODSWe investigated dynamic functional connectivity (dFC), during resting state functional magnetic resonance imaging, between sensorimotor network and top-down control networks in 36 PD patients (OFF medication, PD-OFF) and 36 healthy volunteers. We further assessed the effect of medication on dFC in18 PD patients who were also scanned ON medication.The dFC analyses identified three discrete states: State I (35.68%) characterized by connections between the cerebellum and sensorimotor network, State II (34.17%) with connections between the sensorimotor and frontal-parietal network, and State III (30.15%) with connection between the sensorimotor and cingulo-opercular network. PD patients have significantly fewer occurrences and overall spent less time (shorter dwell time) in State II compared to healthy controls. After levodopa intake, dwell time improved toward normal. The change in dwell time before and after taking levodopa was negatively related to the respective changes in Unified Parkinson's Disease Rating Scale, Part III. PD-OFF showed significantly decreased connectivity between sensorimotor and control networks and increased connectivity within control networks. These changes were partially improved after levodopa intake.RESULTSThe dFC analyses identified three discrete states: State I (35.68%) characterized by connections between the cerebellum and sensorimotor network, State II (34.17%) with connections between the sensorimotor and frontal-parietal network, and State III (30.15%) with connection between the sensorimotor and cingulo-opercular network. PD patients have significantly fewer occurrences and overall spent less time (shorter dwell time) in State II compared to healthy controls. After levodopa intake, dwell time improved toward normal. The change in dwell time before and after taking levodopa was negatively related to the respective changes in Unified Parkinson's Disease Rating Scale, Part III. PD-OFF showed significantly decreased connectivity between sensorimotor and control networks and increased connectivity within control networks. These changes were partially improved after levodopa intake.Dopamine depletion in PD is associated with abnormalities in temporal and spatial properties between cognitive control and sensorimotor network, possibly contributing to clinical deficits. Levodopa partially restores the network function toward the values observed in healthy volunteers. © 2021 International Parkinson and Movement Disorder Society.CONCLUSIONSDopamine depletion in PD is associated with abnormalities in temporal and spatial properties between cognitive control and sensorimotor network, possibly contributing to clinical deficits. Levodopa partially restores the network function toward the values observed in healthy volunteers. © 2021 International Parkinson and Movement Disorder Society.
BackgroundMotor symptoms in Parkinson's disease (PD) patients might be related to high‐level task‐control deficits. We aimed at investigating the dynamics between sensorimotor network and top‐down control networks (frontal–parietal, cingulo‐opercular, and cerebellar) in PD and at determining the effects of levodopa on the dynamics of these networks.MethodsWe investigated dynamic functional connectivity (dFC), during resting state functional magnetic resonance imaging, between sensorimotor network and top‐down control networks in 36 PD patients (OFF medication, PD‐OFF) and 36 healthy volunteers. We further assessed the effect of medication on dFC in18 PD patients who were also scanned ON medication.ResultsThe dFC analyses identified three discrete states: State I (35.68%) characterized by connections between the cerebellum and sensorimotor network, State II (34.17%) with connections between the sensorimotor and frontal–parietal network, and State III (30.15%) with connection between the sensorimotor and cingulo‐opercular network. PD patients have significantly fewer occurrences and overall spent less time (shorter dwell time) in State II compared to healthy controls. After levodopa intake, dwell time improved toward normal. The change in dwell time before and after taking levodopa was negatively related to the respective changes in Unified Parkinson's Disease Rating Scale, Part III. PD‐OFF showed significantly decreased connectivity between sensorimotor and control networks and increased connectivity within control networks. These changes were partially improved after levodopa intake.ConclusionsDopamine depletion in PD is associated with abnormalities in temporal and spatial properties between cognitive control and sensorimotor network, possibly contributing to clinical deficits. Levodopa partially restores the network function toward the values observed in healthy volunteers. © 2021 International Parkinson and Movement Disorder Society
Background Motor symptoms in Parkinson's disease (PD) patients might be related to high‐level task‐control deficits. We aimed at investigating the dynamics between sensorimotor network and top‐down control networks (frontal–parietal, cingulo‐opercular, and cerebellar) in PD and at determining the effects of levodopa on the dynamics of these networks. Methods We investigated dynamic functional connectivity (dFC), during resting state functional magnetic resonance imaging, between sensorimotor network and top‐down control networks in 36 PD patients (OFF medication, PD‐OFF) and 36 healthy volunteers. We further assessed the effect of medication on dFC in18 PD patients who were also scanned ON medication. Results The dFC analyses identified three discrete states: State I (35.68%) characterized by connections between the cerebellum and sensorimotor network, State II (34.17%) with connections between the sensorimotor and frontal–parietal network, and State III (30.15%) with connection between the sensorimotor and cingulo‐opercular network. PD patients have significantly fewer occurrences and overall spent less time (shorter dwell time) in State II compared to healthy controls. After levodopa intake, dwell time improved toward normal. The change in dwell time before and after taking levodopa was negatively related to the respective changes in Unified Parkinson's Disease Rating Scale, Part III. PD‐OFF showed significantly decreased connectivity between sensorimotor and control networks and increased connectivity within control networks. These changes were partially improved after levodopa intake. Conclusions Dopamine depletion in PD is associated with abnormalities in temporal and spatial properties between cognitive control and sensorimotor network, possibly contributing to clinical deficits. Levodopa partially restores the network function toward the values observed in healthy volunteers. © 2021 International Parkinson and Movement Disorder Society
Author Hallett, Mark
Chen, Li
Bedard, Patrick
Horovitz, Silvina G.
AuthorAffiliation 1 Human Motor Control Section, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
2 Department of Radiology, Affiliated Hospital of North Sichuan Medical College, Nanchong, China
AuthorAffiliation_xml – name: 2 Department of Radiology, Affiliated Hospital of North Sichuan Medical College, Nanchong, China
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  surname: Horovitz
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Keywords dynamic functional connectivity
top-down control networks
motor network
Parkinson's disease
dopamine
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SSID ssj0011516
Score 2.5191805
Snippet Background Motor symptoms in Parkinson's disease (PD) patients might be related to high‐level task‐control deficits. We aimed at investigating the dynamics...
Motor symptoms in Parkinson's disease (PD) patients might be related to high-level task-control deficits. We aimed at investigating the dynamics between...
BackgroundMotor symptoms in Parkinson's disease (PD) patients might be related to high‐level task‐control deficits. We aimed at investigating the dynamics...
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SubjectTerms Cerebellum
Cognitive ability
Dopamine
dynamic functional connectivity
Functional magnetic resonance imaging
Humans
Levodopa
Magnetic Resonance Imaging
motor network
Motor task performance
Movement disorders
Neural Pathways - diagnostic imaging
Neurodegenerative diseases
Parkinson Disease - drug therapy
Parkinson's disease
Sensorimotor system
top‐down control networks
Title Dynamics of Top‐Down Control and Motor Networks in Parkinson's Disease
URI https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fmds.28461
https://www.ncbi.nlm.nih.gov/pubmed/33404161
https://www.proquest.com/docview/2512251960
https://www.proquest.com/docview/2475528567
https://pubmed.ncbi.nlm.nih.gov/PMC8373438
Volume 36
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