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

Thomas Blauwblomme, Athena Demertzi, Jean Marc Tacchela, Ludovic Fillon, Marie Bourgeois, Emma Losito, Monika Eisermann, Daniele Marinazzo, Federico Raimondo, Sarael Alcauter, Frederik Van De Steen, Nigel Colenbier, Steven Laureys, Volodia Dangouloff-Ros, Lionel Naccache, Nathalie Boddaert, Rima Nabbout

Onderzoeksoutput: Articlepeer review

2 Citaten (Scopus)

Samenvatting

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.
Originele taal-2English
Pagina's (van-tot)537-549
Aantal pagina's13
TijdschriftEpilepsia Open
Volume5
Nummer van het tijdschrift4
DOI's
StatusPublished - 1 dec 2020

Bibliografische nota

Funding Information:
We are grateful to Dr Antonopoulos Georgios for his contribution with the clinical classifier and the members of the Liège Coma Science Group for their assistance in clinical evaluations of patients with disorders of consciousness. AD is a Research Associate at the Belgian fund for Scientific Research (FRS‐FNRS). FR is a Postdoctoral Researcher supported by the Wallonie‐Bruxelles International IN Excellence Grant. NG is a Research Fellow supported by the Doctoral Fonds Wetenschappelijk Onderzoek Vlaanderen (FWO‐Aspirant). SL is a Research Director at FRS‐FNRS and was further supported by the University and University Hospital of Liège, the European Union's Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement No. 785907 (Human Brain Project SGA2), the Luminous project (EU‐H2020‐fetopenga686764), the European Space Agency (ESA), and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Program, the Center‐TBI project (FP7‐HEALTH‐602150). RN was supported by the EJP‐RD: European Joint Program for rare diseases and the Interface imagine.

Funding Information:
We are grateful to Dr Antonopoulos Georgios for his contribution with the clinical classifier and the members of the Liège Coma Science Group for their assistance in clinical evaluations of patients with disorders of consciousness. AD is a Research Associate at the Belgian fund for Scientific Research (FRS-FNRS). FR is a Postdoctoral Researcher supported by the Wallonie-Bruxelles International IN Excellence Grant. NG is a Research Fellow supported by the Doctoral Fonds Wetenschappelijk Onderzoek Vlaanderen (FWO-Aspirant). SL is a Research Director at FRS-FNRS and was further supported by the University and University Hospital of Liège, the European Union's Horizon 2020 Framework Program for Research and Innovation under the Specific Grant Agreement No. 785907 (Human Brain Project SGA2), the Luminous project (EU-H2020-fetopenga686764), the European Space Agency (ESA), and the Belgian Federal Science Policy Office (BELSPO) in the framework of the PRODEX Program, the Center-TBI project (FP7-HEALTH-602150). RN was supported by the EJP-RD: European Joint Program for rare diseases and the Interface imagine.

Publisher Copyright:
© 2020 The Authors. Epilepsia Open published by Wiley Periodicals LLC on behalf of International League Against Epilepsy

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

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