Progressive dissociation of cortical and subcortical network development in children with new‐onset juvenile myoclonic epilepsy

Garcia‐Ramos, Camille; Dabbs, Kevin; Lin, Jack J.; Jones, Jana E.; Stafstrom, Carl E.; Hsu, David; Meyerand, M. Elizabeth; Prabhakaran, Vivek; Hermann, Bruce P.

doi:10.1111/epi.14560

Cited by 15 publications

(14 citation statements)

References 41 publications

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“…Hubs are the regions that provide valuable information about the configuration of a network. 23 All of these studies have consistently documented cortical and subcortical network abnormalities in patients with JME, and this is in line with our present study. One functional connectivity study based on EEG demonstrated an increased delta, theta, alpha1 connectivity and a decreased alpha2 and beta connectivity in the patients with JME as compared to healthy controls, mainly among cortical areas that were involved in sensory-motor integration.…”

Section: Discussionsupporting

confidence: 93%

Structural and functional connectivity in newly diagnosed juvenile myoclonic epilepsy

Lee

Park

2019

Acta Neurol Scand

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Objectives We aimed to evaluate structural and functional connectivity of patients with newly diagnosed juvenile myoclonic epilepsy (JME) compared to healthy subjects. Methods We enrolled 36 patients with a diagnosis of JME, who were newly diagnosed and drug‐naïve. They underwent T1‐weighted imaging, and structural volumes were calculated using FreeSurfer software. In addition, EEG data were obtained from all of them. Structural and functional connectivity matrices were estimated by calculating the structural volumes and EEG amplitude correlation, respectively. Then, the connectivity measures were calculated using the BRAPH program. We also enrolled healthy subjects to compare its structural and functional connectivity with the patients with JME. Results We observed that patients with JME exhibited significantly different functional and structural connectivity compared to healthy control subjects. In the global structural connectivity, global efficiency, and local efficiency, and small‐worldness index were decreased, whereas characteristic path length was increased in patients with JME. Betweenness centrality of cingulate, precentral, superior parietal, and superior frontal cortex was increased in patients with JME whereas that of hippocampus was decreased. In the functional connectivity, the betweenness centrality of the fronto‐central electrodes was significantly increased. Conclusions This study reports that the structural connectivity and functional connectivity in patients with JME are significantly different from those in healthy control subjects, even those with newly diagnosed drug‐naive state. The patients with JME exhibited disrupted topological disorganization of the global brain network and hub reorganization in structural and functional connectivity. These alterations are implicated in the pathogenesis of JME and suggestive of network disease.

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Section: Discussionsupporting

confidence: 93%

Structural and functional connectivity in newly diagnosed juvenile myoclonic epilepsy

Lee

Park

2019

Acta Neurol Scand

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“…We previously performed similar analyses in youth with juvenile myoclonic epilepsy (JME), and the results revealed a prospective network characterized by highly correlated cortical regions that were unassociated with subcortical structures. Regarding network hubs, JME participants showed half the total number of hubs compared to controls.…”

Section: Discussionmentioning

confidence: 92%

“…Methods for matrix creation and GT measures can be found in a previous investigation . In short, we calculated a weighted undirected matrix of 85 nodes based on the correlation coefficients of the covariance between nodal volume changes for each group.…”

Section: Methodsmentioning

confidence: 99%

“…Methods for matrix creation and GT measures can be found in a previous investigation. 39 In short, we calculated a weighted undirected matrix of 85 nodes based on the correlation coefficients of the covariance between nodal volume changes for each group. Each matrix was resampled by replacement 500 times, and the null distribution was calculated based on 500 random matrices with the same number of nodes and degree distribution as the pertinent graphs.…”

Section: Matrix and Graph Theory Measures: Calculations And Statistmentioning

confidence: 99%

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Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition

et al. 2019

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Objective Benign epilepsy with centrotemporal spikes (BECTS) is the most common childhood idiopathic localization‐related epilepsy syndrome. BECTS presents normal routine magnetic resonance imaging (MRI); however, quantitative analytic techniques have captured subtle cortical and subcortical magnetic resonance anomalies. Network science, including graph theory (GT) analyses, facilitates understanding of brain covariance patterns, potentially informing in important ways how this common self‐limiting epilepsy syndrome may impact normal patterns of brain and cognitive development. Methods GT analyses examined the developmental covariance among cortical and subcortical regions in children with new/recent onset BECTS (n = 19) and typically developing healthy controls (n = 22) who underwent high‐resolution MRI and cognitive assessment at baseline and 2 years later. Global (transitivity, global efficiency, and modularity index [Q]) and regional measures (local efficiency and hubs) were investigated to characterize network development in each group. Associations between baseline‐based GT measures and cognition at both time points addressed the implications of GT analyses for cognition and prospective cognitive development. Furthermore, an individual contribution measure was investigated, reflecting how important for cognition it is for BECTS to resemble the correlation matrices of controls. Results Groups exhibited similar Q and overall network configuration, with BECTS presenting significantly higher transitivity and both global and local efficiency. Furthermore, both groups presented a similar number of hubs, with BECTS showing a higher number in temporal lobe regions compared to controls. The investigated measures were negatively associated with 2‐year cognitive outcomes in BECTS. Significance Children with BECTS present a higher‐than‐normal global developmental configuration compared to controls, along with divergence from normality in terms of regional configuration. Baseline GT measures demonstrate potential as a cognitive biomarker to predict cognitive outcome in BECTS 2 years after diagnosis. Similarities and differences in developmental network configurations and their implications for cognition and behavior across common epilepsy syndromes are of theoretical interest and clinical relevance.

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“…A recent study concerning structural connectivity showed that patients with JME presented lower modularity indices than healthy controls, indicating weaker modules or communities, demonstrating that JME brains were not developing efficiently. 29 However, no studies focused on the intrinsic thalamic network, and we found new information showing increased modularity of the intrinsic thalamic network in patients with JME.…”

Section: Ta B L E 2 (Continued)mentioning

confidence: 70%

Thalamic nuclei volumes and network in juvenile myoclonic epilepsy

et al. 2019

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Objective The aim of this study was to investigate the alterations of thalamic nuclei volumes and intrinsic thalamic networks in patients with juvenile myoclonic epilepsy (JME) compared to healthy controls. Methods We enrolled 50 patients with JME and 42 healthy controls. We obtained structural volumes of the individual thalamic nuclei based on T1‐weighted imaging and performed intrinsic thalamic network analysis using graph theoretical analysis. We analyzed the differences of thalamic nuclei volumes and intrinsic thalamic networks between the patients with JME and healthy controls. Results In the patients with JME, there were significant alterations of thalamic nuclei volumes compared to healthy controls. Right laterodorsal and left suprageniculate nuclei volumes were significantly increased (0.0019% vs 0.0014%, P < .0001; 0.0011% vs 0.0008%, P = .0006, respectively), whereas left ventral posterolateral, left ventromedial, and left pulvinar inferior nuclei volumes (0.0572% vs 0.0664%, P = .0001; 0.0013% vs 0.0015%, P = .0002; 0.0120% vs 0.0140%, P < .0001, respectively) were decreased in the patients with JME. Furthermore, the intrinsic thalamic network of the patients with JME was significantly different from that of the healthy controls. The modularity in the patients with JME was significantly increased over that in healthy controls (0.0785 vs 0.0212, P = .039). Conclusion We found that there were significant alterations of thalamic nuclei volumes and intrinsic thalamic networks in patients with JME compared to healthy controls. These findings might contribute to the underlying pathogenesis of in JME.

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Progressive dissociation of cortical and subcortical network development in children with new‐onset juvenile myoclonic epilepsy

Cited by 15 publications

References 41 publications

Structural and functional connectivity in newly diagnosed juvenile myoclonic epilepsy

Structural and functional connectivity in newly diagnosed juvenile myoclonic epilepsy

Network analysis of prospective brain development in youth with benign epilepsy with centrotemporal spikes and its relationship to cognition

Thalamic nuclei volumes and network in juvenile myoclonic epilepsy

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