Brain functional connectivity in sleep-related hypermotor epilepsy

Objectives: To evaluate functional connectivity (FC) in patients with sleep-related hypermotor epilepsy (SHE) compared to healthy controls. Methods: Resting state fMRI was performed in 13 patients with a clinical diagnosis of SHE (age=38.3±11.8years, 6M) and 13 matched healthy controls (age=38.5±10....

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Main Authors: Stefania Evangelisti, Claudia Testa, Lorenzo Ferri, Laura Ludovica Gramegna, David Neil Manners, Giovanni Rizzo, Daniel Remondini, Gastone Castellani, Ilaria Naldi, Francesca Bisulli, Caterina Tonon, Paolo Tinuper, Raffaele Lodi
Format: Article
Language:English
Published: Elsevier 2018-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158217303078
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author Stefania Evangelisti
Claudia Testa
Lorenzo Ferri
Laura Ludovica Gramegna
David Neil Manners
Giovanni Rizzo
Daniel Remondini
Gastone Castellani
Ilaria Naldi
Francesca Bisulli
Caterina Tonon
Paolo Tinuper
Raffaele Lodi
author_facet Stefania Evangelisti
Claudia Testa
Lorenzo Ferri
Laura Ludovica Gramegna
David Neil Manners
Giovanni Rizzo
Daniel Remondini
Gastone Castellani
Ilaria Naldi
Francesca Bisulli
Caterina Tonon
Paolo Tinuper
Raffaele Lodi
author_sort Stefania Evangelisti
collection DOAJ
description Objectives: To evaluate functional connectivity (FC) in patients with sleep-related hypermotor epilepsy (SHE) compared to healthy controls. Methods: Resting state fMRI was performed in 13 patients with a clinical diagnosis of SHE (age=38.3±11.8years, 6M) and 13 matched healthy controls (age=38.5±10.8years, 6M).Data were first analysed using probabilistic independent component analysis (ICA), then a graph theoretical approach was applied to assess topological and organizational properties at the whole brain level. We evaluated node degree (ND), betweenness centrality (BC), clustering coefficient (CC), local efficiency (LE) and global efficiency (GE). The differences between the two groups were evaluated non-parametrically. Results: At the group level, we distinguished 16 RSNs (Resting State Networks). Patients showed a significantly higher FC in sensorimotor and thalamic regions (p<0.05 corrected). Compared to controls, SHE patients showed no significant differences in network global efficiency, while ND and BC were higher in regions of the limbic system and lower in the occipital cortex, while CC and LE were higher in regions of basal ganglia and lower in limbic areas (p<0.05 uncorrected). Discussion and conclusions: The higher FC of the sensorimotor cortex and thalamus might be in agreement with the hypothesis of a peculiar excitability of the motor cortex during thalamic K-complexes. This sensorimotor-thalamic hyperconnection might be regarded as a consequence of an alteration of the arousal regulatory system in SHE. An altered topology has been found in structures like basal ganglia and limbic system, hypothesized to be involved in the pathophysiology of the disease as suggested by the dystonic-dyskinetic features and primitive behaviours observed during the seizures. Keywords: Sleep-related hypermotor epilepsy, Nocturnal frontal lobe epilepsy, Functional connectivity, Independent component analysis, Graph theory
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spelling doaj.art-c683f2152ecd409b97e33025386f9c222022-12-21T23:53:32ZengElsevierNeuroImage: Clinical2213-15822018-01-0117873881Brain functional connectivity in sleep-related hypermotor epilepsyStefania Evangelisti0Claudia Testa1Lorenzo Ferri2Laura Ludovica Gramegna3David Neil Manners4Giovanni Rizzo5Daniel Remondini6Gastone Castellani7Ilaria Naldi8Francesca Bisulli9Caterina Tonon10Paolo Tinuper11Raffaele Lodi12Functional MR Unit, Policlinico S.Orsola - Malpighi, via Massarenti 9, 40138, Bologna, Italy; Department of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, ItalyFunctional MR Unit, Policlinico S.Orsola - Malpighi, via Massarenti 9, 40138, Bologna, Italy; Department of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, Italy; INFN- National Institute of Nuclear Physics, Bologna, ItalyDepartment of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, Italy; IRCCS Institute of Neurological Sciences of Bologna, via Altura 3, 40139, Bologna, ItalyFunctional MR Unit, Policlinico S.Orsola - Malpighi, via Massarenti 9, 40138, Bologna, Italy; Department of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, ItalyFunctional MR Unit, Policlinico S.Orsola - Malpighi, via Massarenti 9, 40138, Bologna, Italy; Department of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, ItalyDepartment of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, Italy; IRCCS Institute of Neurological Sciences of Bologna, via Altura 3, 40139, Bologna, ItalyINFN- National Institute of Nuclear Physics, Bologna, Italy; Department of Physics and Astronomy, University of Bologna, Bologna, ItalyINFN- National Institute of Nuclear Physics, Bologna, Italy; Department of Physics and Astronomy, University of Bologna, Bologna, ItalyDepartment of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, Italy; IRCCS Institute of Neurological Sciences of Bologna, via Altura 3, 40139, Bologna, ItalyDepartment of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, Italy; IRCCS Institute of Neurological Sciences of Bologna, via Altura 3, 40139, Bologna, ItalyFunctional MR Unit, Policlinico S.Orsola - Malpighi, via Massarenti 9, 40138, Bologna, Italy; Department of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, ItalyDepartment of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, Italy; IRCCS Institute of Neurological Sciences of Bologna, via Altura 3, 40139, Bologna, ItalyFunctional MR Unit, Policlinico S.Orsola - Malpighi, via Massarenti 9, 40138, Bologna, Italy; Department of Biomedical and NeuroMotor Sciences, University of Bologna, via U. Foscolo 7, 40123, Bologna, Italy; Corresponding author at: Functional MR Unit, Policlinico S.Orsola – Malpighi, Department of Biomedical and NeuroMotor Sciences (DiBiNeM), University of Bologna, Via Massarenti 9, 40138 Bologna, Italy.Objectives: To evaluate functional connectivity (FC) in patients with sleep-related hypermotor epilepsy (SHE) compared to healthy controls. Methods: Resting state fMRI was performed in 13 patients with a clinical diagnosis of SHE (age=38.3±11.8years, 6M) and 13 matched healthy controls (age=38.5±10.8years, 6M).Data were first analysed using probabilistic independent component analysis (ICA), then a graph theoretical approach was applied to assess topological and organizational properties at the whole brain level. We evaluated node degree (ND), betweenness centrality (BC), clustering coefficient (CC), local efficiency (LE) and global efficiency (GE). The differences between the two groups were evaluated non-parametrically. Results: At the group level, we distinguished 16 RSNs (Resting State Networks). Patients showed a significantly higher FC in sensorimotor and thalamic regions (p<0.05 corrected). Compared to controls, SHE patients showed no significant differences in network global efficiency, while ND and BC were higher in regions of the limbic system and lower in the occipital cortex, while CC and LE were higher in regions of basal ganglia and lower in limbic areas (p<0.05 uncorrected). Discussion and conclusions: The higher FC of the sensorimotor cortex and thalamus might be in agreement with the hypothesis of a peculiar excitability of the motor cortex during thalamic K-complexes. This sensorimotor-thalamic hyperconnection might be regarded as a consequence of an alteration of the arousal regulatory system in SHE. An altered topology has been found in structures like basal ganglia and limbic system, hypothesized to be involved in the pathophysiology of the disease as suggested by the dystonic-dyskinetic features and primitive behaviours observed during the seizures. Keywords: Sleep-related hypermotor epilepsy, Nocturnal frontal lobe epilepsy, Functional connectivity, Independent component analysis, Graph theoryhttp://www.sciencedirect.com/science/article/pii/S2213158217303078
spellingShingle Stefania Evangelisti
Claudia Testa
Lorenzo Ferri
Laura Ludovica Gramegna
David Neil Manners
Giovanni Rizzo
Daniel Remondini
Gastone Castellani
Ilaria Naldi
Francesca Bisulli
Caterina Tonon
Paolo Tinuper
Raffaele Lodi
Brain functional connectivity in sleep-related hypermotor epilepsy
NeuroImage: Clinical
title Brain functional connectivity in sleep-related hypermotor epilepsy
title_full Brain functional connectivity in sleep-related hypermotor epilepsy
title_fullStr Brain functional connectivity in sleep-related hypermotor epilepsy
title_full_unstemmed Brain functional connectivity in sleep-related hypermotor epilepsy
title_short Brain functional connectivity in sleep-related hypermotor epilepsy
title_sort brain functional connectivity in sleep related hypermotor epilepsy
url http://www.sciencedirect.com/science/article/pii/S2213158217303078
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