Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease

Abstract The aim of the current study was to assess the structural centrality and microstructural integrity of the cortical hubs of the salience network, the anterior insular cortex (AIC) subregions and anterior cingulate cortex (ACC), and their relationship to cognitive and affective impairment in...

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Main Authors: L. E. Jonkman, Y. Y. Fathy, H. W. Berendse, M. M. Schoonheim, W. D. J. van de Berg
Format: Article
Language:English
Published: Nature Publishing Group 2021-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-95638-8
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spelling doaj-571c482d2fc744afb2e2e0039c5413c92021-08-08T11:25:13ZengNature Publishing GroupScientific Reports2045-23222021-08-0111111010.1038/s41598-021-95638-8Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s diseaseL. E. Jonkman0Y. Y. Fathy1H. W. Berendse2M. M. Schoonheim3W. D. J. van de Berg4Department of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit AmsterdamDepartment of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit AmsterdamDepartment of Neurology, Amsterdam UMC - location VUmcDepartment of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit AmsterdamDepartment of Anatomy and Neurosciences, Amsterdam UMC, Vrije Universiteit AmsterdamAbstract The aim of the current study was to assess the structural centrality and microstructural integrity of the cortical hubs of the salience network, the anterior insular cortex (AIC) subregions and anterior cingulate cortex (ACC), and their relationship to cognitive and affective impairment in PD. MRI of 53 PD patients and 15 age-matched controls included 3D-T1 for anatomical registration, and diffusion tensor imaging for probabilistic tractography. Network topological measures of eigenvector and betweenness centrality were calculated for ventral (vAI) and dorsal (dAI) AIC. Microstructural tract integrity between vAI, dAI and the ACC was quantified with fractional anisotrophy (FA) and mean diffusivity (MD). Structural integrity and connectivity were related to cognitive and affective scores. The dAI had significantly higher eigenvector centrality in PD than controls (p < 0.01), associated with higher depression scores (left dAI only, r s  = 0.28, p < 0.05). Tracts between dAI and ACC showed lower FA and higher MD in PD (p < 0.05), and associated with lower semantic fluency, working memory and executive functioning, and higher anxiety scores (range 0.002 < p < 0.05). This study provides evidence for clinically relevant structural damage to the cortical hubs of the salience network in PD, possibly due to extensive local neuropathology and loss of interconnecting AIC-ACC tracts.https://doi.org/10.1038/s41598-021-95638-8
collection DOAJ
language English
format Article
sources DOAJ
author L. E. Jonkman
Y. Y. Fathy
H. W. Berendse
M. M. Schoonheim
W. D. J. van de Berg
spellingShingle L. E. Jonkman
Y. Y. Fathy
H. W. Berendse
M. M. Schoonheim
W. D. J. van de Berg
Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease
Scientific Reports
author_facet L. E. Jonkman
Y. Y. Fathy
H. W. Berendse
M. M. Schoonheim
W. D. J. van de Berg
author_sort L. E. Jonkman
title Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease
title_short Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease
title_full Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease
title_fullStr Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease
title_full_unstemmed Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease
title_sort structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in parkinson’s disease
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2021-08-01
description Abstract The aim of the current study was to assess the structural centrality and microstructural integrity of the cortical hubs of the salience network, the anterior insular cortex (AIC) subregions and anterior cingulate cortex (ACC), and their relationship to cognitive and affective impairment in PD. MRI of 53 PD patients and 15 age-matched controls included 3D-T1 for anatomical registration, and diffusion tensor imaging for probabilistic tractography. Network topological measures of eigenvector and betweenness centrality were calculated for ventral (vAI) and dorsal (dAI) AIC. Microstructural tract integrity between vAI, dAI and the ACC was quantified with fractional anisotrophy (FA) and mean diffusivity (MD). Structural integrity and connectivity were related to cognitive and affective scores. The dAI had significantly higher eigenvector centrality in PD than controls (p < 0.01), associated with higher depression scores (left dAI only, r s  = 0.28, p < 0.05). Tracts between dAI and ACC showed lower FA and higher MD in PD (p < 0.05), and associated with lower semantic fluency, working memory and executive functioning, and higher anxiety scores (range 0.002 < p < 0.05). This study provides evidence for clinically relevant structural damage to the cortical hubs of the salience network in PD, possibly due to extensive local neuropathology and loss of interconnecting AIC-ACC tracts.
url https://doi.org/10.1038/s41598-021-95638-8
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