Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade glioma

Objective: In the event of neural injury, the homologous contralateral brain areas may play a compensatory role to avoid or limit the functional loss. However, this dynamic strategy of functional redistribution is not clearly established, especially in the pathophysiological context of diffuse low-g...

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Main Authors: Fabien Almairac, Jeremy Deverdun, Jérôme Cochereau, Arthur Coget, Anne-Laure Lemaitre, Sylvie Moritz-Gasser, Hugues Duffau, Guillaume Herbet
Format: Article
Language:English
Published: Elsevier 2021-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158221000152
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author Fabien Almairac
Jeremy Deverdun
Jérôme Cochereau
Arthur Coget
Anne-Laure Lemaitre
Sylvie Moritz-Gasser
Hugues Duffau
Guillaume Herbet
author_facet Fabien Almairac
Jeremy Deverdun
Jérôme Cochereau
Arthur Coget
Anne-Laure Lemaitre
Sylvie Moritz-Gasser
Hugues Duffau
Guillaume Herbet
author_sort Fabien Almairac
collection DOAJ
description Objective: In the event of neural injury, the homologous contralateral brain areas may play a compensatory role to avoid or limit the functional loss. However, this dynamic strategy of functional redistribution is not clearly established, especially in the pathophysiological context of diffuse low-grade glioma. Our aim here was to assess the extent to which unilateral tumor infiltration of the insula dynamically modulates the functional connectivity of the contralesional one. Methods: Using resting-state functional connectivity MRI, a seed-to-ROI approach was employed in 52 insula-centered glioma patients (n = 30 left and 22 right) compared with 19 age-matched healthy controls. Results: Unsurprisingly, a significant decrease of the inter-insular connectivity was observed in both patient groups. More importantly, the analyses revealed a significant increase of the contralesional insular connectivity towards both cerebral hemispheres, especially in cortical areas forming the visual and the sensorimotor networks. This functional redistribution was not identified when the analyses were performed on three control regions for which the homologous area was not impaired by the tumor. This overall pattern of results indicates that massive infiltration of the insular cortex causes a significant redeployment of the contralesional functional connectivity. Conclusion: This general finding suggests that the undamaged insula plays a role in the functional compensation usually observed in this patient population, and thus provides compelling support for the concept of homotopic functional plasticity in brain-damaged patients.
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spelling doaj.art-8dccc17431a349c29d82966e5883292b2022-12-21T22:27:25ZengElsevierNeuroImage: Clinical2213-15822021-01-0129102571Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade gliomaFabien Almairac0Jeremy Deverdun1Jérôme Cochereau2Arthur Coget3Anne-Laure Lemaitre4Sylvie Moritz-Gasser5Hugues Duffau6Guillaume Herbet7Department of Neurosurgery, Pasteur 2 Hospital, Nice University Medical Center, Nice, France; Université Côte d’Azur, Nice, FranceI2FH, Institut d'Imagerie Fonctionnelle Humaine, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France; Department of Neuroradiology, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, FranceDepartment of Neurosurgery, La Miletrie Hospital, Poitiers University Medical Center, Poitiers, France; Institute of Functional Genomics, INSERM 1191, University of Montpellier, France; University of Montpellier, Montpellier, FranceI2FH, Institut d'Imagerie Fonctionnelle Humaine, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France; Department of Neuroradiology, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, FranceDepartment of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, FranceInstitute of Functional Genomics, INSERM 1191, University of Montpellier, France; University of Montpellier, Montpellier, France; Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, FranceInstitute of Functional Genomics, INSERM 1191, University of Montpellier, France; University of Montpellier, Montpellier, France; Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, FranceInstitute of Functional Genomics, INSERM 1191, University of Montpellier, France; University of Montpellier, Montpellier, France; Department of Neurosurgery, Gui de Chauliac Hospital, Montpellier University Medical Center, Montpellier, France; Corresponding author at: Department of Neurosurgery, Hôpital Gui de Chauliac, Institute of Functional Genomics, INSERM 1191, University of Montpellier, 80 avenue Augustin Fliche, 34295 Montpellier, France.Objective: In the event of neural injury, the homologous contralateral brain areas may play a compensatory role to avoid or limit the functional loss. However, this dynamic strategy of functional redistribution is not clearly established, especially in the pathophysiological context of diffuse low-grade glioma. Our aim here was to assess the extent to which unilateral tumor infiltration of the insula dynamically modulates the functional connectivity of the contralesional one. Methods: Using resting-state functional connectivity MRI, a seed-to-ROI approach was employed in 52 insula-centered glioma patients (n = 30 left and 22 right) compared with 19 age-matched healthy controls. Results: Unsurprisingly, a significant decrease of the inter-insular connectivity was observed in both patient groups. More importantly, the analyses revealed a significant increase of the contralesional insular connectivity towards both cerebral hemispheres, especially in cortical areas forming the visual and the sensorimotor networks. This functional redistribution was not identified when the analyses were performed on three control regions for which the homologous area was not impaired by the tumor. This overall pattern of results indicates that massive infiltration of the insular cortex causes a significant redeployment of the contralesional functional connectivity. Conclusion: This general finding suggests that the undamaged insula plays a role in the functional compensation usually observed in this patient population, and thus provides compelling support for the concept of homotopic functional plasticity in brain-damaged patients.http://www.sciencedirect.com/science/article/pii/S2213158221000152InsulaPlasticityGliomaHomotopicFunctional MRIFunctional connectivity
spellingShingle Fabien Almairac
Jeremy Deverdun
Jérôme Cochereau
Arthur Coget
Anne-Laure Lemaitre
Sylvie Moritz-Gasser
Hugues Duffau
Guillaume Herbet
Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade glioma
NeuroImage: Clinical
Insula
Plasticity
Glioma
Homotopic
Functional MRI
Functional connectivity
title Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade glioma
title_full Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade glioma
title_fullStr Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade glioma
title_full_unstemmed Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade glioma
title_short Homotopic redistribution of functional connectivity in insula-centered diffuse low-grade glioma
title_sort homotopic redistribution of functional connectivity in insula centered diffuse low grade glioma
topic Insula
Plasticity
Glioma
Homotopic
Functional MRI
Functional connectivity
url http://www.sciencedirect.com/science/article/pii/S2213158221000152
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