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Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase
Previous evidence suggests that the derangement of large-scale brain networks reflects structural, molecular, and functional mechanisms underlying neurodegenerative diseases. Although the alterations of multiple large-scale brain networks in Parkinson’s disease (PD) and Dementia with Lewy Bodies (DL...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9394228/ https://www.ncbi.nlm.nih.gov/pubmed/36003959 http://dx.doi.org/10.3389/fnins.2022.930735 |
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author | Boccalini, Cecilia Bortolin, Elisa Carli, Giulia Pilotto, Andrea Galbiati, Andrea Padovani, Alessandro Ferini-Strambi, Luigi Perani, Daniela |
author_facet | Boccalini, Cecilia Bortolin, Elisa Carli, Giulia Pilotto, Andrea Galbiati, Andrea Padovani, Alessandro Ferini-Strambi, Luigi Perani, Daniela |
author_sort | Boccalini, Cecilia |
collection | PubMed |
description | Previous evidence suggests that the derangement of large-scale brain networks reflects structural, molecular, and functional mechanisms underlying neurodegenerative diseases. Although the alterations of multiple large-scale brain networks in Parkinson’s disease (PD) and Dementia with Lewy Bodies (DLB) are reported, a comprehensive study on connectivity reconfiguration starting from the preclinical phase is still lacking. We aimed to investigate shared and disease-specific changes in the large-scale networks across the Lewy Bodies (LB) disorders spectrum using a brain metabolic connectivity approach. We included 30 patients with isolated REM sleep behavior disorder (iRBD), 28 with stable PD, 30 with DLB, and 30 healthy controls for comparison. We applied seed-based interregional correlation analyses (IRCA) to evaluate the metabolic connectivity in the large-scale resting-state networks, as assessed by [18F]FDG-PET, in each clinical group compared to controls. We assessed metabolic connectivity changes by applying the IRCA and specific connectivity metrics, such as the weighted and unweighted Dice similarity coefficients (DC), for the topographical similarities. All the investigated large-scale brain resting-state networks showed metabolic connectivity alterations, supporting the widespread involvement of brain connectivity within the alpha-synuclein spectrum. Connectivity alterations were already evident in iRBD, severely affecting the posterior default mode, attentive and limbic networks. Strong similarities emerged in iRBD and DLB that showed comparable connectivity alterations in most large-scale networks, particularly in the posterior default mode and attentive networks. Contrarily, PD showed the main connectivity alterations limited to motor and somatosensory networks. The present findings reveal that metabolic connectivity alterations in the large-scale networks are already present in the early iRBD phase, resembling the DLB metabolic connectivity changes. This suggests and confirms iRBD as a risk condition for progression to the severe LB disease phenotype. Of note, the neurobiology of stable PD supports its more benign phenotype. |
format | Online Article Text |
id | pubmed-9394228 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-93942282022-08-23 Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase Boccalini, Cecilia Bortolin, Elisa Carli, Giulia Pilotto, Andrea Galbiati, Andrea Padovani, Alessandro Ferini-Strambi, Luigi Perani, Daniela Front Neurosci Neuroscience Previous evidence suggests that the derangement of large-scale brain networks reflects structural, molecular, and functional mechanisms underlying neurodegenerative diseases. Although the alterations of multiple large-scale brain networks in Parkinson’s disease (PD) and Dementia with Lewy Bodies (DLB) are reported, a comprehensive study on connectivity reconfiguration starting from the preclinical phase is still lacking. We aimed to investigate shared and disease-specific changes in the large-scale networks across the Lewy Bodies (LB) disorders spectrum using a brain metabolic connectivity approach. We included 30 patients with isolated REM sleep behavior disorder (iRBD), 28 with stable PD, 30 with DLB, and 30 healthy controls for comparison. We applied seed-based interregional correlation analyses (IRCA) to evaluate the metabolic connectivity in the large-scale resting-state networks, as assessed by [18F]FDG-PET, in each clinical group compared to controls. We assessed metabolic connectivity changes by applying the IRCA and specific connectivity metrics, such as the weighted and unweighted Dice similarity coefficients (DC), for the topographical similarities. All the investigated large-scale brain resting-state networks showed metabolic connectivity alterations, supporting the widespread involvement of brain connectivity within the alpha-synuclein spectrum. Connectivity alterations were already evident in iRBD, severely affecting the posterior default mode, attentive and limbic networks. Strong similarities emerged in iRBD and DLB that showed comparable connectivity alterations in most large-scale networks, particularly in the posterior default mode and attentive networks. Contrarily, PD showed the main connectivity alterations limited to motor and somatosensory networks. The present findings reveal that metabolic connectivity alterations in the large-scale networks are already present in the early iRBD phase, resembling the DLB metabolic connectivity changes. This suggests and confirms iRBD as a risk condition for progression to the severe LB disease phenotype. Of note, the neurobiology of stable PD supports its more benign phenotype. Frontiers Media S.A. 2022-08-08 /pmc/articles/PMC9394228/ /pubmed/36003959 http://dx.doi.org/10.3389/fnins.2022.930735 Text en Copyright © 2022 Boccalini, Bortolin, Carli, Pilotto, Galbiati, Padovani, Ferini-Strambi and Perani. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Neuroscience Boccalini, Cecilia Bortolin, Elisa Carli, Giulia Pilotto, Andrea Galbiati, Andrea Padovani, Alessandro Ferini-Strambi, Luigi Perani, Daniela Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase |
title | Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase |
title_full | Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase |
title_fullStr | Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase |
title_full_unstemmed | Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase |
title_short | Metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase |
title_sort | metabolic connectivity of resting-state networks in alpha synucleinopathies, from prodromal to dementia phase |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9394228/ https://www.ncbi.nlm.nih.gov/pubmed/36003959 http://dx.doi.org/10.3389/fnins.2022.930735 |
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