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Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy

Rolandic epilepsy (RE) is the most common focal, idiopathic, developmental epilepsy, characterized by a transient period of sleep-potentiated seizures and epileptiform discharges in the inferior Rolandic cortex during childhood. The cause of RE remains unknown but converging evidence has identified...

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Autores principales: Kwon, Hunki, Chinappen, Dhinakaran M., Huang, Jonathan F., Berja, Erin D., Walsh, Katherine G., Wen, Shi, Kramer, Mark A., Chu, Catherine J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9251597/
https://www.ncbi.nlm.nih.gov/pubmed/35777251
http://dx.doi.org/10.1016/j.nicl.2022.103102
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author Kwon, Hunki
Chinappen, Dhinakaran M.
Huang, Jonathan F.
Berja, Erin D.
Walsh, Katherine G.
Wen, Shi
Kramer, Mark A.
Chu, Catherine J.
author_facet Kwon, Hunki
Chinappen, Dhinakaran M.
Huang, Jonathan F.
Berja, Erin D.
Walsh, Katherine G.
Wen, Shi
Kramer, Mark A.
Chu, Catherine J.
author_sort Kwon, Hunki
collection PubMed
description Rolandic epilepsy (RE) is the most common focal, idiopathic, developmental epilepsy, characterized by a transient period of sleep-potentiated seizures and epileptiform discharges in the inferior Rolandic cortex during childhood. The cause of RE remains unknown but converging evidence has identified abnormalities in the Rolandic thalamocortical circuit. To better localize this transient disease, we evaluated Rolandic thalamocortical functional and structural connectivity in the sensory and motor circuits separately during the symptomatic and asymptomatic phases of this disease. We collected high resolution structural, diffusion, and resting state functional MRI data in a prospective cohort of children with active RE (n = 17), resolved RE (n = 21), and controls (n = 33). We then computed the functional and structural connectivity between the inferior Rolandic cortex and the ventrolateral (VL) nucleus of the thalamus (efferent pathway) and the ventroposterolateral (VPL) nucleus of the thalamus (afferent pathway) across development in children with active, resolved RE and controls. We compared connectivity with age in each group using linear mixed-effects models. We found that children with active RE have increasing thalamocortical functional connectivity between the VL thalamus and inferior motor cortex with age (p = 0.022) that is not observed in controls or resolved RE. In contrast, children with resolved RE have increasing thalamocortical structural connectivity between the VL nucleus and the inferior motor cortex with age (p = 0.025) that is not observed in controls or active RE. No relationships were identified between VPL nuclei and the inferior sensory cortex with age in any group. These findings localize the functional and structural thalamocortical circuit disruption in RE to the efferent thalamocortical motor pathway. Further work is required to determine how these circuit abnormalities contribute to the emergence and resolution of symptoms in this developmental disease.
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spelling pubmed-92515972022-07-05 Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy Kwon, Hunki Chinappen, Dhinakaran M. Huang, Jonathan F. Berja, Erin D. Walsh, Katherine G. Wen, Shi Kramer, Mark A. Chu, Catherine J. Neuroimage Clin Regular Article Rolandic epilepsy (RE) is the most common focal, idiopathic, developmental epilepsy, characterized by a transient period of sleep-potentiated seizures and epileptiform discharges in the inferior Rolandic cortex during childhood. The cause of RE remains unknown but converging evidence has identified abnormalities in the Rolandic thalamocortical circuit. To better localize this transient disease, we evaluated Rolandic thalamocortical functional and structural connectivity in the sensory and motor circuits separately during the symptomatic and asymptomatic phases of this disease. We collected high resolution structural, diffusion, and resting state functional MRI data in a prospective cohort of children with active RE (n = 17), resolved RE (n = 21), and controls (n = 33). We then computed the functional and structural connectivity between the inferior Rolandic cortex and the ventrolateral (VL) nucleus of the thalamus (efferent pathway) and the ventroposterolateral (VPL) nucleus of the thalamus (afferent pathway) across development in children with active, resolved RE and controls. We compared connectivity with age in each group using linear mixed-effects models. We found that children with active RE have increasing thalamocortical functional connectivity between the VL thalamus and inferior motor cortex with age (p = 0.022) that is not observed in controls or resolved RE. In contrast, children with resolved RE have increasing thalamocortical structural connectivity between the VL nucleus and the inferior motor cortex with age (p = 0.025) that is not observed in controls or active RE. No relationships were identified between VPL nuclei and the inferior sensory cortex with age in any group. These findings localize the functional and structural thalamocortical circuit disruption in RE to the efferent thalamocortical motor pathway. Further work is required to determine how these circuit abnormalities contribute to the emergence and resolution of symptoms in this developmental disease. Elsevier 2022-06-27 /pmc/articles/PMC9251597/ /pubmed/35777251 http://dx.doi.org/10.1016/j.nicl.2022.103102 Text en © 2022 The Author(s) https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
Kwon, Hunki
Chinappen, Dhinakaran M.
Huang, Jonathan F.
Berja, Erin D.
Walsh, Katherine G.
Wen, Shi
Kramer, Mark A.
Chu, Catherine J.
Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy
title Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy
title_full Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy
title_fullStr Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy
title_full_unstemmed Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy
title_short Transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in Rolandic epilepsy
title_sort transient, developmental functional and structural connectivity abnormalities in the thalamocortical motor network in rolandic epilepsy
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9251597/
https://www.ncbi.nlm.nih.gov/pubmed/35777251
http://dx.doi.org/10.1016/j.nicl.2022.103102
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