Relationship Between Seizure Frequency and Functional Abnormalities in Limbic Network of Medial Temporal Lobe Epilepsy

Jo, Hang Joon; Kenney‐Jung, Daniel L.; Balzekas, Irena; Welker, Kirk M.; Jones, David T.; Croarkin, Paul E.; Benarroch, Eduardo E.; Worrell, Gregory A.

doi:10.3389/fneur.2019.00488

Cited by 33 publications

(30 citation statements)

References 34 publications

(30 reference statements)

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“…Thus, we could not control for the effects of AED or seizure frequency, which can affect the thalamic nuclei volumes and intrinsic thalamic network. 30,31 Further longitudinal studies with large sample size may be needed to confirm our findings. Second, we analyzed thalamic nuclei volumes and network based on thalamic nuclei volumes using the latest version of FreeSurfer program.…”

Section: Ta B L E 2 (Continued)mentioning

confidence: 55%

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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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Section: Ta B L E 2 (Continued)mentioning

confidence: 55%

“…Furthermore, we enrolled patients with chronic epilepsy as well as newly diagnosed epilepsy. Thus, we could not control for the effects of AED or seizure frequency, which can affect the thalamic nuclei volumes and intrinsic thalamic network . Further longitudinal studies with large sample size may be needed to confirm our findings.…”

Section: Discussionmentioning

confidence: 76%

Thalamic nuclei volumes and network in juvenile myoclonic epilepsy

et al. 2019

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“…Through this approach, we were able to show that while the Limbic and Frontoparietal Networks, both previously described in clinical experience in people with epilepsy 33,34 , continued to show a high likelihood of being functionally connected with EL_INSTs, the Dorsal and Ventral Attention Networks along with the DMN were in fact more likely to be functionally connected with NEL_INSTs. The areas within the Limbic Network play a key role in epilepsy secondary to their ability to produce and propagate synchronized physiological activity 35,[36][37][38][39] . Furthermore, structural changes in the thalamus (part of the limbic network), including loss of volume over time, have been reported in various forms of epilepsy suggesting the critical role of this structure within a broader epilepsy network 32,40,41 .…”

Section: Discussionmentioning

confidence: 99%

Identification of neural networks preferentially engaged by epileptogenic mass lesions through lesion network mapping analysis

Mansouri

Germann

Boutet

et al. 2020

Sci Rep

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Lesion network mapping (LNM) has been applied to true lesions (e.g., cerebrovascular lesions in stroke) to identify functionally connected brain networks. No previous studies have utilized LNM for analysis of intra-axial mass lesions. Here, we implemented LNM for identification of potentially vulnerable epileptogenic networks in mass lesions causing medically-refractory epilepsy (MRE). Intra-axial brain lesions were manually segmented in patients with MRE seen at our institution (EL_ INST). These lesions were then normalized to standard space and used as seeds in a high-resolution normative resting state functional magnetic resonance imaging template. The resulting connectivity maps were first thresholded (p Bonferroni_cor < 0.05) and binarized; the thresholded binarized connectivity maps were subsequently summed to produce overall group connectivity maps, which were compared with established resting-state networks to identify potential networks prone to epileptogenicity. To validate our data, this approach was also applied to an external dataset of epileptogenic lesions identified from the literature (EL_LIT). As an additional exploratory analysis, we also segmented and computed the connectivity of institutional non-epileptogenic lesions (NEL_INST), calculating voxelwise odds ratios (VORs) to identify voxels more likely to be functionally-connected with EL_INST versus NEL_INST. To ensure connectivity results were not driven by anatomical overlap, the extent of lesion overlap between EL_INST, and EL_LIT and NEL_INST was assessed using the Dice Similarity Coefficient (DSC, lower index ~ less overlap). Twenty-eight patients from our institution were included (EL_INST: 17 patients, 17 lesions, 10 low-grade glioma, 3 cavernoma, 4 focal cortical dysplasia; NEL_ INST: 11 patients, 33 lesions, all brain metastases). An additional 23 cases (25 lesions) with similar characteristics to the EL_INST data were identified from the literature (EL_LIT). Despite minimal anatomical overlap of lesions, both EL_INST and EL_LIT showed greatest functional connectivity overlap with structures in the Default Mode Network, Frontoparietal Network, Ventral Attention Network, and the Limbic Network-with percentage volume overlap of 19.5%, 19.1%, 19.1%, and 12.5%, respectively-suggesting them as networks consistently engaged by epileptogenic mass lesions. Our exploratory analysis moreover showed that the mesial frontal lobes, parahippocampal gyrus, and lateral temporal neocortex were at least twice as likely to be functionally connected with the EL_INST compared to the NEL_INST group (i.e. Peak VOR > 2.0); canonical resting-state

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“…A functional MRI (fMRI) study revealed that decreased regional homogeneity was present primarily in the default mode network (DMN; including the precuneus, the posterior CG and the mesial prefrontal cortex) in patients with TLE, relative to the HC subjects (14). In another fMRI study, functional network abnormalities were identified in the limbic systems of patients with TLE (including the ipsilateral ventral anterior cingulate cortex and the hypothalamus, the subiculum and the posterior cingulate cortex), which was significantly correlated with seizure frequency (3). In neuroimaging studies, functional and structural alterations are frequently observed in the cingulate cortex of patients with TLE.…”

Section: Introductionmentioning

confidence: 92%

“…TLE is associated with various cognitive impairments such as attention deficit and memory impairment, and impacts patient quality of life. Recurrent abnormal neuronal discharges accelerate the risk of abnormal lesions in a number of brain regions, including the temporal and extratemporal regions, which may contribute to their functional impairment (3). However, the underlying pathophysiological and neurological mechanisms of TLE have remained elusive.…”

Section: Introductionmentioning

confidence: 99%

Aberrant functional connectivity of the cingulate subregions in right‑sided temporal lobe epilepsy

et al. 2020

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Patients with temporal lobe epilepsy (TLE) have been indicated to exhibit abnormal resting-state functional connectivity (rsFC) of the cingulate cortex. However, it has remained elusive whether cingulate subregions show different connectivity patterns in TLE. The present study aimed to investigate the differences in rsFC of each cingulate subregion between patients with right-sided TLE (rTLE) and healthy controls (HCs), as well as their association with executive control performance in rTLE. A total of 27 patients with rTLE and 20 age-, sex-and education-matched healthy controls were recruited and all participants underwent resting-state functional MRI and an attention network test for the assessment executive control function. In each hemisphere, the cingulate gyrus (CG) was divided into CG-1 (dorsal area 23; A23d), CG-2 (rostroventral area 24; A24rv), CG-3 (pregenual area 32; A32p), CG-4 (ventral area 23; A23v), CG-5 (caudodorsal area 24; A24cd), CG-6 (caudal area 24; A23c) and CG-7 (subgenual area 32; A32sg). Pearson's correlation analysis was performed to assess the correlation between the altered FCs of the cingulate subregions and clinical variables. In patients with rTLE, the majority of the cingulate subregions exhibited decreased rsFC; this was primarily restricted to the right CG-2, the bilateral CG-6 and the bilateral CG-7. Increased rsFC was only detected in rTLE restricted to the left CG-1. Impairments in executive control efficiency were identified in patients with rTLE in comparison with the HCs. Significant alterations in rsFC between the cingulate subregion and the brain regions were mostly decreased (and some slightly increased), suggesting that FC may potentially have a left-side advantage in patients with rTLE. FC variations of the cingulate subregions were indicated to be specific to rTLE. In addition, increased connectivity in the left CG-1 and left superior frontal gyrus were negatively correlated with executive control performance, suggesting a compensatory mechanism on executive control deficits in pathological conditions. This information on differentially altered FC patterns of the cingulate subregions may provide a deeper understanding of the complex neurological mechanisms and executive control dysfunctions underlying rTLE.

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Relationship Between Seizure Frequency and Functional Abnormalities in Limbic Network of Medial Temporal Lobe Epilepsy

Cited by 33 publications

References 34 publications

Thalamic nuclei volumes and network in juvenile myoclonic epilepsy

Thalamic nuclei volumes and network in juvenile myoclonic epilepsy

Identification of neural networks preferentially engaged by epileptogenic mass lesions through lesion network mapping analysis

Aberrant functional connectivity of the cingulate subregions in right‑sided temporal lobe epilepsy

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