Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's Disease

The phenomenon of impulsivity in Parkinson's disease appears as an arduous side effect of dopaminergic therapy with potentially detrimental consequences for the life of the patients. Although conceptualized as a result of non-physiologic chronic dopaminergic stimulation, recent advances specula...

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Main Authors: Pavel Filip, Pavla Linhartová, Pavlína Hlavatá, Rastislav Šumec, Marek Baláž, Martin Bareš, Tomáš Kašpárek
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-11-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2018.00462/full
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author Pavel Filip
Pavel Filip
Pavla Linhartová
Pavlína Hlavatá
Rastislav Šumec
Marek Baláž
Martin Bareš
Martin Bareš
Tomáš Kašpárek
author_facet Pavel Filip
Pavel Filip
Pavla Linhartová
Pavlína Hlavatá
Rastislav Šumec
Marek Baláž
Martin Bareš
Martin Bareš
Tomáš Kašpárek
author_sort Pavel Filip
collection DOAJ
description The phenomenon of impulsivity in Parkinson's disease appears as an arduous side effect of dopaminergic therapy with potentially detrimental consequences for the life of the patients. Although conceptualized as a result of non-physiologic chronic dopaminergic stimulation, recent advances speculate on combined disruption of other networks as well. In the search for neuroanatomical correlates of this multifaceted disturbance, this study employs two distinct, well-defined tasks of close association to motor inhibition and decision-making impulsivity, Go/No Go and Delay discounting. The fMRI and functional connectivity analysis in 21 Parkinson's disease patients, including 8 patients suffering from severe impulse control disorder, and 28 healthy controls, revealed in impulsive Parkinson's disease patients not only decreased fMRI activation in the dorsolateral prefrontal cortex and bilateral striatum, but also vast functional connectivity changes of both caudate nuclei as decreased connectivity to the superior parietal cortex and increased connectivity to the insular area, clearly beyond the commonly stated areas, which indicates that orbitofronto-striatal and mesolimbic functional disruptions are not the sole mechanisms underlying impulse control disorder in Parkinson's disease. Ergo, our results present a refinement and synthesis of gradually developing ideas about the nature of impulsive control disorder in Parkinson's disease—an umbrella term encompassing various behavioral deviations related to distinct neuronal networks and presumably neurotransmitter systems, which greatly exceed the previously envisioned dopaminergic pathways as the only culprit.
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spelling doaj.art-d511d60b8df043e0a324ceb91384f3fc2022-12-22T00:45:19ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612018-11-011210.3389/fnhum.2018.00462405866Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's DiseasePavel Filip0Pavel Filip1Pavla Linhartová2Pavlína Hlavatá3Rastislav Šumec4Marek Baláž5Martin Bareš6Martin Bareš7Tomáš Kašpárek8First Department of Neurology, Faculty of Medicine, Masaryk University and University Hospital of St. Anne, Brno, CzechiaCenter for Magnetic Resonance Research (CMRR), University of Minnesota, Minneapolis, MN, United StatesDepartment of Psychiatry, Faculty of Medicine, Masaryk University and University Hospital Brno, Brno, CzechiaDepartment of Psychiatry, Faculty of Medicine, Masaryk University and University Hospital Brno, Brno, CzechiaFirst Department of Neurology, Faculty of Medicine, Masaryk University and University Hospital of St. Anne, Brno, CzechiaFirst Department of Neurology, Faculty of Medicine, Masaryk University and University Hospital of St. Anne, Brno, CzechiaFirst Department of Neurology, Faculty of Medicine, Masaryk University and University Hospital of St. Anne, Brno, CzechiaDepartment of Neurology, School of Medicine, University of Minnesota, Minneapolis, MN, United StatesDepartment of Psychiatry, Faculty of Medicine, Masaryk University and University Hospital Brno, Brno, CzechiaThe phenomenon of impulsivity in Parkinson's disease appears as an arduous side effect of dopaminergic therapy with potentially detrimental consequences for the life of the patients. Although conceptualized as a result of non-physiologic chronic dopaminergic stimulation, recent advances speculate on combined disruption of other networks as well. In the search for neuroanatomical correlates of this multifaceted disturbance, this study employs two distinct, well-defined tasks of close association to motor inhibition and decision-making impulsivity, Go/No Go and Delay discounting. The fMRI and functional connectivity analysis in 21 Parkinson's disease patients, including 8 patients suffering from severe impulse control disorder, and 28 healthy controls, revealed in impulsive Parkinson's disease patients not only decreased fMRI activation in the dorsolateral prefrontal cortex and bilateral striatum, but also vast functional connectivity changes of both caudate nuclei as decreased connectivity to the superior parietal cortex and increased connectivity to the insular area, clearly beyond the commonly stated areas, which indicates that orbitofronto-striatal and mesolimbic functional disruptions are not the sole mechanisms underlying impulse control disorder in Parkinson's disease. Ergo, our results present a refinement and synthesis of gradually developing ideas about the nature of impulsive control disorder in Parkinson's disease—an umbrella term encompassing various behavioral deviations related to distinct neuronal networks and presumably neurotransmitter systems, which greatly exceed the previously envisioned dopaminergic pathways as the only culprit.https://www.frontiersin.org/article/10.3389/fnhum.2018.00462/fullimpulse control disorderParkinson's diseasefMRIfunctional connectivityGo/No Go taskdelay discounting task
spellingShingle Pavel Filip
Pavel Filip
Pavla Linhartová
Pavlína Hlavatá
Rastislav Šumec
Marek Baláž
Martin Bareš
Martin Bareš
Tomáš Kašpárek
Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's Disease
Frontiers in Human Neuroscience
impulse control disorder
Parkinson's disease
fMRI
functional connectivity
Go/No Go task
delay discounting task
title Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's Disease
title_full Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's Disease
title_fullStr Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's Disease
title_full_unstemmed Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's Disease
title_short Disruption of Multiple Distinctive Neural Networks Associated With Impulse Control Disorder in Parkinson's Disease
title_sort disruption of multiple distinctive neural networks associated with impulse control disorder in parkinson s disease
topic impulse control disorder
Parkinson's disease
fMRI
functional connectivity
Go/No Go task
delay discounting task
url https://www.frontiersin.org/article/10.3389/fnhum.2018.00462/full
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