Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging data

Background: Impulse control behaviors (ICB) are frequently observed in patients with Parkinson’s disease (PD) and are characterized by compulsive and repetitive behavior resulting from the inability to resist internal drives. Objectives: In this study, we aimed to provide a better understanding of s...

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Main Authors: Hamzah Baagil, Christian Hohenfeld, Ute Habel, Simon B. Eickhoff, Raquel E. Gur, Kathrin Reetz, Imis Dogan
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158223000049
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author Hamzah Baagil
Christian Hohenfeld
Ute Habel
Simon B. Eickhoff
Raquel E. Gur
Kathrin Reetz
Imis Dogan
author_facet Hamzah Baagil
Christian Hohenfeld
Ute Habel
Simon B. Eickhoff
Raquel E. Gur
Kathrin Reetz
Imis Dogan
author_sort Hamzah Baagil
collection DOAJ
description Background: Impulse control behaviors (ICB) are frequently observed in patients with Parkinson’s disease (PD) and are characterized by compulsive and repetitive behavior resulting from the inability to resist internal drives. Objectives: In this study, we aimed to provide a better understanding of structural and functional brain alterations and clinical parameters related to ICB in PD patients. Methods: We utilized a dataset from the Parkinson’s Progression Markers Initiative including 36 patients with ICB (PDICB+) compared to 76 without ICB (PDICB-) and 61 healthy controls (HC). Using multimodal MRI data we assessed gray matter brain volume, white matter integrity, and graph topological properties at rest. Results: Compared with HC, PDICB+ showed reduced gray matter volume in the bilateral superior and middle temporal gyrus and in the right middle occipital gyrus. Compared with PDICB-, PDICB+ showed volume reduction in the left anterior insula. Depression and anxiety were more prevalent in PDICB+ than in PDICB- and HC. In PDICB+, lower gray matter volume in the precentral gyrus and medial frontal cortex, and higher axial diffusivity in the superior corona radiata were related to higher depression score. Both PD groups showed disrupted functional topological network pattern within the cingulate cortex compared with HC. PDICB+ vs PDICB- displayed reduced topological network pattern in the anterior cingulate cortex, insula, and nucleus accumbens. Conclusions: Our results suggest that structural alterations in the insula and abnormal topological connectivity pattern in the salience network and the nucleus accumbens may lead to impaired decision making and hypersensitivity towards reward in PDICB+. Moreover, PDICB+ are more prone to suffer from depression and anxiety.
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spelling doaj.art-0fdeca8a8ca5498596c0ac9ec8446c1f2023-03-16T05:04:02ZengElsevierNeuroImage: Clinical2213-15822023-01-0137103315Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging dataHamzah Baagil0Christian Hohenfeld1Ute Habel2Simon B. Eickhoff3Raquel E. Gur4Kathrin Reetz5Imis Dogan6Department of Neurology, RWTH Aachen University, Pauwelsstraße 30, Aachen, Germany; JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich and RWTH Aachen University, GermanyDepartment of Neurology, RWTH Aachen University, Pauwelsstraße 30, Aachen, Germany; JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich and RWTH Aachen University, GermanyDepartment of Psychiatry, Psychotherapy and Psychosomatics, RWTH Aachen University, Pauwelsstraße 30, Aachen, Germany; JARA‑BRAIN, Jülich‑Aachen Research Alliance, Institute of Brain Structure-Function Relationships, Aachen, GermanyInstitute for Systems Neuroscience, Medical Faculty, Heinrich-Heine University, Düsseldorf, Germany; Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Research Center Jülich, GermanyDepartment of Psychiatry, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USADepartment of Neurology, RWTH Aachen University, Pauwelsstraße 30, Aachen, Germany; JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich and RWTH Aachen University, Germany; Corresponding author at: Department of Neurology, RWTH Aachen University, Pauwelsstraße 30, 52074 Aachen, Germany.Department of Neurology, RWTH Aachen University, Pauwelsstraße 30, Aachen, Germany; JARA-BRAIN Institute Molecular Neuroscience and Neuroimaging, Research Center Jülich and RWTH Aachen University, GermanyBackground: Impulse control behaviors (ICB) are frequently observed in patients with Parkinson’s disease (PD) and are characterized by compulsive and repetitive behavior resulting from the inability to resist internal drives. Objectives: In this study, we aimed to provide a better understanding of structural and functional brain alterations and clinical parameters related to ICB in PD patients. Methods: We utilized a dataset from the Parkinson’s Progression Markers Initiative including 36 patients with ICB (PDICB+) compared to 76 without ICB (PDICB-) and 61 healthy controls (HC). Using multimodal MRI data we assessed gray matter brain volume, white matter integrity, and graph topological properties at rest. Results: Compared with HC, PDICB+ showed reduced gray matter volume in the bilateral superior and middle temporal gyrus and in the right middle occipital gyrus. Compared with PDICB-, PDICB+ showed volume reduction in the left anterior insula. Depression and anxiety were more prevalent in PDICB+ than in PDICB- and HC. In PDICB+, lower gray matter volume in the precentral gyrus and medial frontal cortex, and higher axial diffusivity in the superior corona radiata were related to higher depression score. Both PD groups showed disrupted functional topological network pattern within the cingulate cortex compared with HC. PDICB+ vs PDICB- displayed reduced topological network pattern in the anterior cingulate cortex, insula, and nucleus accumbens. Conclusions: Our results suggest that structural alterations in the insula and abnormal topological connectivity pattern in the salience network and the nucleus accumbens may lead to impaired decision making and hypersensitivity towards reward in PDICB+. Moreover, PDICB+ are more prone to suffer from depression and anxiety.http://www.sciencedirect.com/science/article/pii/S2213158223000049Parkinson’s diseaseImpulse control behaviorsStructural magnetic resonance imaging (MRI)Functional MRI
spellingShingle Hamzah Baagil
Christian Hohenfeld
Ute Habel
Simon B. Eickhoff
Raquel E. Gur
Kathrin Reetz
Imis Dogan
Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging data
NeuroImage: Clinical
Parkinson’s disease
Impulse control behaviors
Structural magnetic resonance imaging (MRI)
Functional MRI
title Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging data
title_full Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging data
title_fullStr Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging data
title_full_unstemmed Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging data
title_short Neural correlates of impulse control behaviors in Parkinson’s disease: Analysis of multimodal imaging data
title_sort neural correlates of impulse control behaviors in parkinson s disease analysis of multimodal imaging data
topic Parkinson’s disease
Impulse control behaviors
Structural magnetic resonance imaging (MRI)
Functional MRI
url http://www.sciencedirect.com/science/article/pii/S2213158223000049
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