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Widespread cortical functional disconnection in gliomas: an individual network mapping approach

Assessment of impaired/preserved cortical regions in brain tumours is typically performed via intraoperative direct brain stimulation of eloquent areas or task-based functional MRI. One main limitation is that they overlook distal brain regions or networks that could be functionally impaired by the...

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Autores principales: Silvestri, Erica, Moretto, Manuela, Facchini, Silvia, Castellaro, Marco, Anglani, Mariagiulia, Monai, Elena, D’Avella, Domenico, Della Puppa, Alessandro, Cecchin, Diego, Bertoldo, Alessandra, Corbetta, Maurizio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9034119/
https://www.ncbi.nlm.nih.gov/pubmed/35474856
http://dx.doi.org/10.1093/braincomms/fcac082
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author Silvestri, Erica
Moretto, Manuela
Facchini, Silvia
Castellaro, Marco
Anglani, Mariagiulia
Monai, Elena
D’Avella, Domenico
Della Puppa, Alessandro
Cecchin, Diego
Bertoldo, Alessandra
Corbetta, Maurizio
author_facet Silvestri, Erica
Moretto, Manuela
Facchini, Silvia
Castellaro, Marco
Anglani, Mariagiulia
Monai, Elena
D’Avella, Domenico
Della Puppa, Alessandro
Cecchin, Diego
Bertoldo, Alessandra
Corbetta, Maurizio
author_sort Silvestri, Erica
collection PubMed
description Assessment of impaired/preserved cortical regions in brain tumours is typically performed via intraoperative direct brain stimulation of eloquent areas or task-based functional MRI. One main limitation is that they overlook distal brain regions or networks that could be functionally impaired by the tumour. This study aims (i) to investigate the impact of brain tumours on the cortical synchronization of brain networks measured with resting-state functional magnetic resonance imaging (resting-state networks) both near the lesion and remotely and (ii) to test whether potential changes in resting-state networks correlate with cognitive status. The sample included 24 glioma patients (mean age: 58.1 ± 16.4 years) with different pathological staging. We developed a new method for single subject localization of resting-state networks abnormalities. First, we derived the spatial pattern of the main resting-state networks by means of the group-guided independent component analysis. This was informed by a high-resolution resting-state networks template derived from an independent sample of healthy controls. Second, we developed a spatial similarity index to measure differences in network topography and strength between healthy controls and individual brain tumour patients. Next, we investigated the spatial relationship between altered networks and tumour location. Finally, multivariate analyses related cognitive scores across multiple cognitive domains (attention, language, memory, decision making) with patterns of multi-network abnormality. We found that brain gliomas cause broad alterations of resting-state networks topography that occurred mainly in structurally normal regions outside the tumour and oedema region. Cortical regions near the tumour often showed normal synchronization. Finally, multi-network abnormalities predicted attention deficits. Overall, we present a novel method for the functional localization of resting-state networks abnormalities in individual glioma patients. These abnormalities partially explain cognitive disabilities and shall be carefully navigated during surgery.
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spelling pubmed-90341192022-04-25 Widespread cortical functional disconnection in gliomas: an individual network mapping approach Silvestri, Erica Moretto, Manuela Facchini, Silvia Castellaro, Marco Anglani, Mariagiulia Monai, Elena D’Avella, Domenico Della Puppa, Alessandro Cecchin, Diego Bertoldo, Alessandra Corbetta, Maurizio Brain Commun Original Article Assessment of impaired/preserved cortical regions in brain tumours is typically performed via intraoperative direct brain stimulation of eloquent areas or task-based functional MRI. One main limitation is that they overlook distal brain regions or networks that could be functionally impaired by the tumour. This study aims (i) to investigate the impact of brain tumours on the cortical synchronization of brain networks measured with resting-state functional magnetic resonance imaging (resting-state networks) both near the lesion and remotely and (ii) to test whether potential changes in resting-state networks correlate with cognitive status. The sample included 24 glioma patients (mean age: 58.1 ± 16.4 years) with different pathological staging. We developed a new method for single subject localization of resting-state networks abnormalities. First, we derived the spatial pattern of the main resting-state networks by means of the group-guided independent component analysis. This was informed by a high-resolution resting-state networks template derived from an independent sample of healthy controls. Second, we developed a spatial similarity index to measure differences in network topography and strength between healthy controls and individual brain tumour patients. Next, we investigated the spatial relationship between altered networks and tumour location. Finally, multivariate analyses related cognitive scores across multiple cognitive domains (attention, language, memory, decision making) with patterns of multi-network abnormality. We found that brain gliomas cause broad alterations of resting-state networks topography that occurred mainly in structurally normal regions outside the tumour and oedema region. Cortical regions near the tumour often showed normal synchronization. Finally, multi-network abnormalities predicted attention deficits. Overall, we present a novel method for the functional localization of resting-state networks abnormalities in individual glioma patients. These abnormalities partially explain cognitive disabilities and shall be carefully navigated during surgery. Oxford University Press 2022-04-08 /pmc/articles/PMC9034119/ /pubmed/35474856 http://dx.doi.org/10.1093/braincomms/fcac082 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Silvestri, Erica
Moretto, Manuela
Facchini, Silvia
Castellaro, Marco
Anglani, Mariagiulia
Monai, Elena
D’Avella, Domenico
Della Puppa, Alessandro
Cecchin, Diego
Bertoldo, Alessandra
Corbetta, Maurizio
Widespread cortical functional disconnection in gliomas: an individual network mapping approach
title Widespread cortical functional disconnection in gliomas: an individual network mapping approach
title_full Widespread cortical functional disconnection in gliomas: an individual network mapping approach
title_fullStr Widespread cortical functional disconnection in gliomas: an individual network mapping approach
title_full_unstemmed Widespread cortical functional disconnection in gliomas: an individual network mapping approach
title_short Widespread cortical functional disconnection in gliomas: an individual network mapping approach
title_sort widespread cortical functional disconnection in gliomas: an individual network mapping approach
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9034119/
https://www.ncbi.nlm.nih.gov/pubmed/35474856
http://dx.doi.org/10.1093/braincomms/fcac082
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