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Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere

OBJECTIVE: To quantify whole‐brain functional organization after complete hemispherotomy, characterizing unexplored plasticity pathways and the conscious level of the dissected hemispheres. METHODS: Evaluation with multimodal magnetic resonance imaging in two pediatric patients undergoing right hemi...

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Autores principales: Blauwblomme, Thomas, Demertzi, Athena, Tacchela, Jean‐Marc, Fillon, Ludovic, Bourgeois, Marie, Losito, Emma, Eisermann, Monika, Marinazzo, Daniele, Raimondo, Federico, Alcauter, Sarael, Van De Steen, Frederik, Colenbier, Nigel, Laureys, Steven, Dangouloff‐Ros, Volodia, Naccache, Lionel, Boddaert, Nathalie, Nabbout, Rima
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7733653/
https://www.ncbi.nlm.nih.gov/pubmed/33336125
http://dx.doi.org/10.1002/epi4.12433
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author Blauwblomme, Thomas
Demertzi, Athena
Tacchela, Jean‐Marc
Fillon, Ludovic
Bourgeois, Marie
Losito, Emma
Eisermann, Monika
Marinazzo, Daniele
Raimondo, Federico
Alcauter, Sarael
Van De Steen, Frederik
Colenbier, Nigel
Laureys, Steven
Dangouloff‐Ros, Volodia
Naccache, Lionel
Boddaert, Nathalie
Nabbout, Rima
author_facet Blauwblomme, Thomas
Demertzi, Athena
Tacchela, Jean‐Marc
Fillon, Ludovic
Bourgeois, Marie
Losito, Emma
Eisermann, Monika
Marinazzo, Daniele
Raimondo, Federico
Alcauter, Sarael
Van De Steen, Frederik
Colenbier, Nigel
Laureys, Steven
Dangouloff‐Ros, Volodia
Naccache, Lionel
Boddaert, Nathalie
Nabbout, Rima
author_sort Blauwblomme, Thomas
collection PubMed
description OBJECTIVE: To quantify whole‐brain functional organization after complete hemispherotomy, characterizing unexplored plasticity pathways and the conscious level of the dissected hemispheres. METHODS: Evaluation with multimodal magnetic resonance imaging in two pediatric patients undergoing right hemispherotomy including complete callosotomy with a perithalamic section. Regional cerebral blood flow and fMRI network connectivity assessed the functional integrity of both hemispheres after surgery. The level of consciousness was tested by means of a support vector machine classifier which compared the intrinsic organization of the dissected hemispheres with those of patients suffering from disorders of consciousness. RESULTS: After hemispherotomy, both patients showed typical daily functionality. We found no interhemispheric transfer of functional connectivity in either patient as predicted by the operation. The healthy left hemispheres displayed focal blood hyperperfusion in motor and limbic areas, with preserved network‐level organization. Unexpectedly, the disconnected right hemispheres showed sustained network organization despite low regional cerebral blood flow. Subcortically, functional connectivity was increased in the left thalamo‐cortical loop and between the cerebelli. One patient further showed unusual ipsilateral right cerebello‐cortical connectivity, which was explained by the mediation of the vascular system. The healthy left hemisphere had higher probability to be classified as in a minimally conscious state compared to the isolated right hemisphere. SIGNIFICANCE: Complete hemispherotomy leads to a lateralized whole‐brain organization, with the remaining hemisphere claiming most of the brain's energetic reserves supported by subcortical structures. Our results further underline the contribution of nonneuronal vascular signals on contralateral connectivity, shedding light on the nature of network organization in the isolated tissue. The disconnected hemisphere is characterized by a level of consciousness which is necessary but insufficient for conscious processing, paving the way for more specific inquiries about its role in awareness in the absence of behavioral output.
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spelling pubmed-77336532020-12-16 Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere Blauwblomme, Thomas Demertzi, Athena Tacchela, Jean‐Marc Fillon, Ludovic Bourgeois, Marie Losito, Emma Eisermann, Monika Marinazzo, Daniele Raimondo, Federico Alcauter, Sarael Van De Steen, Frederik Colenbier, Nigel Laureys, Steven Dangouloff‐Ros, Volodia Naccache, Lionel Boddaert, Nathalie Nabbout, Rima Epilepsia Open Full‐length Original Research OBJECTIVE: To quantify whole‐brain functional organization after complete hemispherotomy, characterizing unexplored plasticity pathways and the conscious level of the dissected hemispheres. METHODS: Evaluation with multimodal magnetic resonance imaging in two pediatric patients undergoing right hemispherotomy including complete callosotomy with a perithalamic section. Regional cerebral blood flow and fMRI network connectivity assessed the functional integrity of both hemispheres after surgery. The level of consciousness was tested by means of a support vector machine classifier which compared the intrinsic organization of the dissected hemispheres with those of patients suffering from disorders of consciousness. RESULTS: After hemispherotomy, both patients showed typical daily functionality. We found no interhemispheric transfer of functional connectivity in either patient as predicted by the operation. The healthy left hemispheres displayed focal blood hyperperfusion in motor and limbic areas, with preserved network‐level organization. Unexpectedly, the disconnected right hemispheres showed sustained network organization despite low regional cerebral blood flow. Subcortically, functional connectivity was increased in the left thalamo‐cortical loop and between the cerebelli. One patient further showed unusual ipsilateral right cerebello‐cortical connectivity, which was explained by the mediation of the vascular system. The healthy left hemisphere had higher probability to be classified as in a minimally conscious state compared to the isolated right hemisphere. SIGNIFICANCE: Complete hemispherotomy leads to a lateralized whole‐brain organization, with the remaining hemisphere claiming most of the brain's energetic reserves supported by subcortical structures. Our results further underline the contribution of nonneuronal vascular signals on contralateral connectivity, shedding light on the nature of network organization in the isolated tissue. The disconnected hemisphere is characterized by a level of consciousness which is necessary but insufficient for conscious processing, paving the way for more specific inquiries about its role in awareness in the absence of behavioral output. John Wiley and Sons Inc. 2020-09-24 /pmc/articles/PMC7733653/ /pubmed/33336125 http://dx.doi.org/10.1002/epi4.12433 Text en © 2020 The Authors. Epilepsia Open published by Wiley Periodicals LLC on behalf of International League Against Epilepsy This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Full‐length Original Research
Blauwblomme, Thomas
Demertzi, Athena
Tacchela, Jean‐Marc
Fillon, Ludovic
Bourgeois, Marie
Losito, Emma
Eisermann, Monika
Marinazzo, Daniele
Raimondo, Federico
Alcauter, Sarael
Van De Steen, Frederik
Colenbier, Nigel
Laureys, Steven
Dangouloff‐Ros, Volodia
Naccache, Lionel
Boddaert, Nathalie
Nabbout, Rima
Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere
title Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere
title_full Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere
title_fullStr Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere
title_full_unstemmed Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere
title_short Complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere
title_sort complete hemispherotomy leads to lateralized functional organization and lower level of consciousness in the isolated hemisphere
topic Full‐length Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7733653/
https://www.ncbi.nlm.nih.gov/pubmed/33336125
http://dx.doi.org/10.1002/epi4.12433
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