Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study

Many studies have used functional magnetic resonance imaging to unravel the neuronal underpinnings of motor system abnormalities in Parkinson's disease, indicating functional inhibition at the level of basal ganglia-thalamo-cortical motor networks. The study aim was to extend the characterizati...

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Main Authors: Jason A. Martin, Nadine Zimmermann, Lukas Scheef, Jakob Jankowski, Sebastian Paus, Hans H. Schild, Thomas Klockgether, Henning Boecker
Format: Article
Language:English
Published: Elsevier 2019-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158219301342
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author Jason A. Martin
Nadine Zimmermann
Lukas Scheef
Jakob Jankowski
Sebastian Paus
Hans H. Schild
Thomas Klockgether
Henning Boecker
author_facet Jason A. Martin
Nadine Zimmermann
Lukas Scheef
Jakob Jankowski
Sebastian Paus
Hans H. Schild
Thomas Klockgether
Henning Boecker
author_sort Jason A. Martin
collection DOAJ
description Many studies have used functional magnetic resonance imaging to unravel the neuronal underpinnings of motor system abnormalities in Parkinson's disease, indicating functional inhibition at the level of basal ganglia-thalamo-cortical motor networks. The study aim was to extend the characterization of functional motor changes in Parkinson's Disease by dissociating between two phases of action (i.e. motor planning and motor execution) during an automated unilateral finger movement sequence with the left and right hand, separately. In essence, we wished to identify neuronal dysfunction and potential neuronal compensation before (planning) and during (execution) automated sequential motor behavior in unmedicated early stage Parkinson's Disease patients. Twenty-two Parkinson's Disease patients (14 males; 53 ± 11 years; Hoehn and Yahr score 1.4 ± 0.6; UPDRS (part 3) motor score 16 ± 6) and 22 healthy controls (14 males; 49 ± 12 years) performed a pre-learnt four finger sequence (index, ring, middle and little finger, in order), either self-initiated (FREE) or externally triggered (REACT), within an 8-second time window. Findings were most pronounced during FREE with the clinically most affected side, where motor execution revealed significant underactivity of contralateral primary motor cortex, contralateral posterior putamen (sensorimotor territory), ipsilateral anterior cerebellum / cerebellar vermis, along with underactivity in supplementary motor area (based on ROI analyses only), corroborating previous findings in Parkinson's Disease. During motor planning, Parkinson's Disease patients showed a significant relative overactivity in dorsolateral prefrontal cortex (DLPFC), suggesting a compensatory overactivity. To a variable extent this relative overactivity in the DLPFC went along with a relative overactivity in the precuneus and the ipsilateral anterior cerebellum/cerebellar vermis Our study illustrates that a refined view of disturbances in motor function and compensatory processes can be gained from experimental designs that try to dissociate motor planning from motor execution, emphasizing that compensatory mechanisms are triggered in Parkinson's Disease when voluntary movements are conceptualized for action. Keywords: Parkinson's disease, Self-initiated movement, Functional MRI, Motor networks, Compensation, Basal ganglia
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spelling doaj.art-0cb1c5caac01439a80ef2504a4bff2372022-12-22T00:43:04ZengElsevierNeuroImage: Clinical2213-15822019-01-0122Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI studyJason A. Martin0Nadine Zimmermann1Lukas Scheef2Jakob Jankowski3Sebastian Paus4Hans H. Schild5Thomas Klockgether6Henning Boecker7Functional Neuroimaging Group, Department of Radiology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany; Deutsches Zentrum für Neurodegenerative Erkrankungen (DZNE), University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany; Corresponding author at: FE Klinische Funktionelle Neurobildgebung, Experimentelle Radiologie, Radiologische Universitätsklinik Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany.Functional Neuroimaging Group, Department of Radiology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany; Department of Neurology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, GermanyFunctional Neuroimaging Group, Department of Radiology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany; Deutsches Zentrum für Neurodegenerative Erkrankungen (DZNE), University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, GermanyFunctional Neuroimaging Group, Department of Radiology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, GermanyDepartment of Neurology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, GermanyDepartment of Radiology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, GermanyDepartment of Neurology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany; Deutsches Zentrum für Neurodegenerative Erkrankungen (DZNE), University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, GermanyFunctional Neuroimaging Group, Department of Radiology, University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, Germany; Deutsches Zentrum für Neurodegenerative Erkrankungen (DZNE), University Hospital Bonn, Sigmund-Freud-Str. 25, 53127 Bonn, GermanyMany studies have used functional magnetic resonance imaging to unravel the neuronal underpinnings of motor system abnormalities in Parkinson's disease, indicating functional inhibition at the level of basal ganglia-thalamo-cortical motor networks. The study aim was to extend the characterization of functional motor changes in Parkinson's Disease by dissociating between two phases of action (i.e. motor planning and motor execution) during an automated unilateral finger movement sequence with the left and right hand, separately. In essence, we wished to identify neuronal dysfunction and potential neuronal compensation before (planning) and during (execution) automated sequential motor behavior in unmedicated early stage Parkinson's Disease patients. Twenty-two Parkinson's Disease patients (14 males; 53 ± 11 years; Hoehn and Yahr score 1.4 ± 0.6; UPDRS (part 3) motor score 16 ± 6) and 22 healthy controls (14 males; 49 ± 12 years) performed a pre-learnt four finger sequence (index, ring, middle and little finger, in order), either self-initiated (FREE) or externally triggered (REACT), within an 8-second time window. Findings were most pronounced during FREE with the clinically most affected side, where motor execution revealed significant underactivity of contralateral primary motor cortex, contralateral posterior putamen (sensorimotor territory), ipsilateral anterior cerebellum / cerebellar vermis, along with underactivity in supplementary motor area (based on ROI analyses only), corroborating previous findings in Parkinson's Disease. During motor planning, Parkinson's Disease patients showed a significant relative overactivity in dorsolateral prefrontal cortex (DLPFC), suggesting a compensatory overactivity. To a variable extent this relative overactivity in the DLPFC went along with a relative overactivity in the precuneus and the ipsilateral anterior cerebellum/cerebellar vermis Our study illustrates that a refined view of disturbances in motor function and compensatory processes can be gained from experimental designs that try to dissociate motor planning from motor execution, emphasizing that compensatory mechanisms are triggered in Parkinson's Disease when voluntary movements are conceptualized for action. Keywords: Parkinson's disease, Self-initiated movement, Functional MRI, Motor networks, Compensation, Basal gangliahttp://www.sciencedirect.com/science/article/pii/S2213158219301342
spellingShingle Jason A. Martin
Nadine Zimmermann
Lukas Scheef
Jakob Jankowski
Sebastian Paus
Hans H. Schild
Thomas Klockgether
Henning Boecker
Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study
NeuroImage: Clinical
title Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study
title_full Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study
title_fullStr Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study
title_full_unstemmed Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study
title_short Disentangling motor planning and motor execution in unmedicated de novo Parkinson's disease patients: An fMRI study
title_sort disentangling motor planning and motor execution in unmedicated de novo parkinson s disease patients an fmri study
url http://www.sciencedirect.com/science/article/pii/S2213158219301342
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