Alterations in the hippocampal‐thalamic pathway underlying secondarily generalized tonic–clonic seizures in mesial temporal lobe epilepsy: A diffusion tensor imaging study

Chen, Cong; Li, Hong; Ding, Fang; Yang, Linglin; Huang, Peiyu; Wang, Shan; Jin, Bo; Xu, Cenglin; Wang, Yi; Ding, Meiping; Chen, Zhong; Wang, Shuang

doi:10.1111/epi.14614

Cited by 31 publications

(29 citation statements)

References 51 publications

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“…From the thalamocortical projections, the excitatory seizure activity propagates to widespread areas after the inhibitory process fails at the basal ganglia 12,17 . Structural and functional abnormalities have been reported in these areas in patients with FBTCS 12,14–16,20 . This hypothesis about the propagation model of FBTCS has primarily been supported by studies incorporating functional imaging modalities and/or T1‐weighted MRI.…”

Section: Discussionmentioning

confidence: 99%

“…This hypothesis about the propagation model of FBTCS has primarily been supported by studies incorporating functional imaging modalities and/or T1‐weighted MRI. Surprisingly, only a few studies have utilized diffusion MRI to study FBTCS, limiting its application to thalamus‐associated fiber bundles 14,16 . We utilized diffusion MRI to study the whole‐brain structural network in FBTCS.…”

Section: Discussionmentioning

confidence: 99%

“…Recognizing the need to quantify patient susceptibility to FBTCS, some studies have investigated a range of clinical factors to differentiate patients with and without FBTCS, 7,11 showing positive association with the presence of hippocampal sclerosis and negative association with ictal speech and pedal automatism 7 . Many studies have suggested that impairments in specific brain regions support FBTCS, after finding disrupted structure and function in circuits mediated by thalamus and basal ganglia 6,12–18 . It has also been suggested that FBTCS have a different mechanism to primary generalized seizures, with more complex patient‐specific spread 10,19–23 .…”

Section: Introductionmentioning

confidence: 99%

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Focal to bilateral tonic–clonic seizures are associated with widespread network abnormality in temporal lobe epilepsy

et al. 2021

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Objective Our objective was to identify whether the whole‐brain structural network alterations in patients with temporal lobe epilepsy (TLE) and focal to bilateral tonic–clonic seizures (FBTCS) differ from alterations in patients without FBTCS. Methods We dichotomized a cohort of 83 drug‐resistant patients with TLE into those with and without FBTCS and compared each group to 29 healthy controls. For each subject, we used diffusion‐weighted magnetic resonance imaging to construct whole‐brain structural networks. First, we measured the extent of alterations by performing FBTCS‐negative (FBTCS−) versus control and FBTCS‐positive (FBTCS+) versus control comparisons, thereby delineating altered subnetworks of the whole‐brain structural network. Second, by standardizing each patient's networks using control networks, we measured the subject‐specific abnormality at every brain region in the network, thereby quantifying the spatial localization and the amount of abnormality in every patient. Results Both FBTCS+ and FBTCS− patient groups had altered subnetworks with reduced fractional anisotropy and increased mean diffusivity compared to controls. The altered subnetwork in FBTCS+ patients was more widespread than in FBTCS− patients (441 connections altered at t > 3, p < .001 in FBTCS+ compared to 21 connections altered at t > 3, p = .01 in FBTCS−). Significantly greater abnormalities—aggregated over the entire brain network as well as assessed at the resolution of individual brain areas—were present in FBTCS+ patients (p < .001, d = .82, 95% confidence interval = .32–1.3). In contrast, the fewer abnormalities present in FBTCS− patients were mainly localized to the temporal and frontal areas. Significance The whole‐brain structural network is altered to a greater and more widespread extent in patients with TLE and FBTCS. We suggest that these abnormal networks may serve as an underlying structural basis or consequence of the greater seizure spread observed in FBTCS.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Focal to bilateral tonic–clonic seizures are associated with widespread network abnormality in temporal lobe epilepsy

et al. 2021

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“…12 Recent work also identified impairment of thalamotemporal structural connections in TLE-FBTCS. 13 The thalamus contributes to motor planning, language and memory by promoting cortical synchronization and facilitating cortico-cortical interplay. 14,15 Cognitive tasks perturb brain network dynamics and evoke complex changes in interregional interactions, 16 offering a powerful tool to identify disease-specific network traits 17 that resting-state analyses may not adequately capture.…”

Section: Introductionmentioning

confidence: 99%

“… 12 Recent work also identified impairment of thalamotemporal structural connections in TLE-FBTCS. 13 …”

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confidence: 99%

Thalamus and focal to bilateral seizures

Caciagli

Allen

et al. 2020

Neurology

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ObjectiveTo investigate the functional correlates of recurrent secondarily generalized seizures in temporal lobe epilepsy (TLE), using task-based fMRI as a framework to test for epilepsy-specific network rearrangements. As the thalamus modulates propagation of temporal-lobe onset seizures and promotes cortical synchronization during cognition, we hypothesized that occurrence of secondarily generalized, i.e.,. focal to bilateral tonic-clonic seizures (FBTCS), would relate to thalamic dysfunction, altered connectivity and whole-brain network centrality.MethodsFBTCS occur in a third of patients with TLE and are a major determinant of disease severity. In this cross-sectional study, we analyzed 113 patients with drug-resistant TLE (55 left/58 right), who performed a verbal fluency fMRI task that elicited robust thalamic activation. Thirty-three patients (29%) had experienced at least one FBTCS in the year preceding the investigation. We compared patients with TLE-FBTCS to those without FBTCS via a multi-scale approach, entailing analysis of SPM12-derived measures of activation, task-modulated thalamic functional connectivity (psychophysiological interaction), and graph-theoretical metrics of centrality.ResultsIndividuals with TLE-FBTCS had less task-related activation of bilateral thalamus, with left-sided emphasis, and left hippocampus than those without FBTCS. In TLE-FBTCS, we also found greater task-related thalamotemporal and thalamo-motor connectivity, and higher thalamic degree and betweenness centrality. Receiver operating characteristic curves, based on a combined thalamic functional marker, accurately discriminated individuals with and without FBTCS.ConclusionsIn TLE-FBTCS, impaired task-related thalamic recruitment coexists with enhanced thalamotemporal connectivity and whole-brain thalamic network embedding. Altered thalamic functional profiles are proposed as imaging biomarkers of active secondary generalization.

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Altered structural network in temporal lobe epilepsy with focal to bilateral tonic–clonic seizures

Ge,

Chen,

et al. 2024

Ann Clin Transl Neurol

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ObjectivesThis study aims to investigate whether alterations in white matter topological networks are associated with focal to bilateral tonic–clonic seizures (FBTCS) in temporal lobe epilepsy (TLE). Additionally, we investigated the variables contributing to memory impairment in TLE.MethodsThis cross‐sectional study included 88 unilateral people with TLE (45 left/43 right), and 42 healthy controls. Graph theory analysis was employed to compare the FBTCS (+) group (n = 51) with the FBTCS (−) group (n = 37). The FBTCS (+) group was subcategorized into current‐FBTCS (n = 31) and remote‐FBTCS (n = 20), based on the history of FBTCS within 1 year or longer than 1 year before scanning, respectively. We evaluated the discriminatory power of topological network properties by receiver operating characteristic (ROC) analysis. Generalized linear models (GLMs) were employed to investigate variables associated with memory impairment in TLE.ResultsGlobal efficiency (Eg) was significantly reduced in the FBTCS (+) group, especially in the current‐FBTCS subgroup. Greater disruption of regional properties in the ipsilateral occipital and temporal association cortices was observed in the FBTCS (+) group. ROC analysis revealed that Eg, normalized characteristic shortest path length, and nodal efficiency of the ipsilateral middle temporal gyrus could distinguish between FBTCS (+) and FBTCS (−) groups. Additionally, GLMs linked the occurrence of current FBTCS with poorer verbal memory outcomes in TLE.InterpretationOur study suggests that abnormal networks could be the structural basis of seizure propagation in FBTCS. Strategies aimed at reducing the occurrence of FBTCS could potentially improve the memory outcomes in people with TLE.

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Alterations in the hippocampal‐thalamic pathway underlying secondarily generalized tonic–clonic seizures in mesial temporal lobe epilepsy: A diffusion tensor imaging study

Cited by 31 publications

References 51 publications

Focal to bilateral tonic–clonic seizures are associated with widespread network abnormality in temporal lobe epilepsy

Focal to bilateral tonic–clonic seizures are associated with widespread network abnormality in temporal lobe epilepsy

Thalamus and focal to bilateral seizures

Altered structural network in temporal lobe epilepsy with focal to bilateral tonic–clonic seizures

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