The anterior and pulvinar thalamic nuclei interactions in mesial temporal lobe seizure networks

Soulier, Hugo; Pizzo, Francesca; Jegou, Aude; Lagarde, Stanislas; Garnier, Élodie; Makhalova, Julia; Villalon, Samuel Médina; Carron, Romain; Bénar, Christian; Bartolomei, Fabricē

doi:10.1016/j.clinph.2023.03.016

Cited by 13 publications

(8 citation statements)

References 27 publications

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“…Recent work on intracranial recordings of temporal lobe epilepsy demonstrated increased connectivity between the anterior nucleus and the pulvinar nucleus during seizures, suggesting that both thalamic nuclei are active nodes in the epileptogenic network. 48 Furthermore, although the anterior nucleus of the thalamus remains a popular target for DBS stimulation, the centromedian and pulvinar nucleus have both been demonstrated as successful targets, although not in a randomized control trial. 21,49 Although preliminary, our findings could have implications for the DBS treatment of L-TLE and R-TLE, as a pulvinar/centromedian stimulation approach could be more appropriate for R-TLE, whereas anterior nucleus stimulation could be more appropriate for L-TLE.…”

Section: Discussionmentioning

confidence: 99%

“…Our findings show that L‐TLE appears to predominantly have atrophy in the ipsilateral hippocampus and anterior thalamus (the focal network mentioned above), whereas R‐TLE appears to predominantly have atrophy in the posteromedial thalamus (centromedian and pulvinar nucleus). Recent work on intracranial recordings of temporal lobe epilepsy demonstrated increased connectivity between the anterior nucleus and the pulvinar nucleus during seizures, suggesting that both thalamic nuclei are active nodes in the epileptogenic network 48 . Furthermore, although the anterior nucleus of the thalamus remains a popular target for DBS stimulation, the centromedian and pulvinar nucleus have both been demonstrated as successful targets, although not in a randomized control trial 21,49 .…”

Section: Discussionmentioning

confidence: 99%

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Mapping hippocampal and thalamic atrophy in epilepsy: A 7‐T magnetic resonance imaging study

Lucas,

Mouchtaris,

Tranquille

et al. 2024

Epilepsia

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ObjectiveEpilepsy patients are often grouped together by clinical variables. Quantitative neuroimaging metrics can provide a data‐driven alternative for grouping of patients. In this work, we leverage ultra‐high‐field 7‐T structural magnetic resonance imaging (MRI) to characterize volumetric atrophy patterns across hippocampal subfields and thalamic nuclei in drug‐resistant focal epilepsy.MethodsForty‐two drug‐resistant epilepsy patients and 13 controls with 7‐T structural neuroimaging were included in this study. We measured hippocampal subfield and thalamic nuclei volumetry, and applied an unsupervised machine learning algorithm, Latent Dirichlet Allocation (LDA), to estimate atrophy patterns across the hippocampal subfields and thalamic nuclei of patients. We studied the association between predefined clinical groups and the estimated atrophy patterns. Additionally, we used hierarchical clustering on the LDA factors to group patients in a data‐driven approach.ResultsIn patients with mesial temporal sclerosis (MTS), we found a significant decrease in volume across all ipsilateral hippocampal subfields (false discovery rate‐corrected p [pFDR] < .01) as well as in some ipsilateral (pFDR < .05) and contralateral (pFDR < .01) thalamic nuclei. In left temporal lobe epilepsy (L‐TLE) we saw ipsilateral hippocampal and some bilateral thalamic atrophy (pFDR < .05), whereas in right temporal lobe epilepsy (R‐TLE) extensive bilateral hippocampal and thalamic atrophy was observed (pFDR < .05). Atrophy factors demonstrated that our MTS cohort had two atrophy phenotypes: one that affected the ipsilateral hippocampus and one that affected the ipsilateral hippocampus and bilateral anterior thalamus. Atrophy factors demonstrated posterior thalamic atrophy in R‐TLE, whereas an anterior thalamic atrophy pattern was more common in L‐TLE. Finally, hierarchical clustering of atrophy patterns recapitulated clusters with homogeneous clinical properties.SignificanceLeveraging 7‐T MRI, we demonstrate widespread hippocampal and thalamic atrophy in epilepsy. Through unsupervised machine learning, we demonstrate patterns of volumetric atrophy that vary depending on disease subtype. Incorporating these atrophy patterns into clinical practice could help better stratify patients to surgical treatments and specific device implantation strategies.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Mapping hippocampal and thalamic atrophy in epilepsy: A 7‐T magnetic resonance imaging study

Lucas,

Mouchtaris,

Tranquille

et al. 2024

Epilepsia

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“…3 Node strength increased during all seizure periods, and this result was in line with previous publications. 11 Despite this global result, there was a great heterogeneity in the FC patterns between patients and even between the different seizures of the same patient. This could be due to the heterogenicity in patients with NH-related drug-resistant epilepsy, with significant variability in the location, the number of NHs, the epilepsy duration before SEEG, and the type of seizures.…”

Section: Discussionmentioning

confidence: 99%

“…We calculated for each channel the mean of the h 2 values of (1) all ingoing links (node IN-strength), (2) all outgoing links (node OUT-strength), (3) the sum of the node IN-and OUT-strength (node total strength = TOTstrength) divided by the number of channels per patient, as described previously. 11 The mean node strength of BG was subtracted from the other periods (OS, MS, and ES) to better estimate the changes in FC due to seizures activity.…”

Section: Functional Connectivity and Epileptogenic Index Analysismentioning

confidence: 99%

Stereo‐EEG–based ictal functional connectivity in patients with periventricular nodular heterotopia–related epilepsy

Zanello,

Garnier,

Carron

et al. 2024

Epilepsia

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Nodular heterotopia (NH)–related drug‐resistant epilepsy is challenging due to the deep location of the NH and the complexity of the underlying epileptogenic network. Using ictal stereo‐electroencephalography (SEEG) and functional connectivity (FC) analyses in 14 patients with NH‐related drug‐resistant epilepsy, we aimed to determine the leading structure during seizures. For this purpose, we compared node IN and OUT strength between bipolar channels inside the heterotopia and inside gray matter, at the group level and at the individual level. At seizure onset, the channels within NH belonging to the epileptogenic and/or propagation network showed higher node OUT‐strength than the channels within the gray matter (p = .03), with higher node OUT‐strength than node IN‐strength (p = .03). These results are in favor of a “leading” role of NH during seizure onset when involved in the epileptogenic‐ or propagation‐zone network (50% of patients). However, when looking at the individual level, no significant difference between NH and gray matter was found, except for one patient (in two of three seizures). This result confirms the heterogeneity and the complexity of the epileptogenic network organization in NH and the need for SEEG exploration to characterize more precisely patient‐specific epileptogenic network organization.

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“…The degree of thalamic involvement significantly affected the post-surgical outcome (higher involvement, higher probability of surgical failure) 9 . Functional connectivity (FC) studies showed a significant involvement of the thalamus in loss of consciousness during seizures (11) and in seizure termination [10][11][12] . These data strongly support the thalamus as a pivotal hub in focal epilepsy, underscoring its relevance for comprehending not only the mechanisms of epileptogenicity but also for exploring therapeutic options such as deep brain stimulation (DBS).…”

Section: Introductionmentioning

confidence: 99%

Interictal waking and sleep electrophysiological properties of the thalamus in focal epilepsies

Biagioni,

Fratello,

Garnier

et al. 2024

Preprint

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Introduction: Addressing drug-resistant epilepsy poses a significant clinical hurdle, particularly when conventional resective surgery is not feasible. Deep brain stimulation (DBS) emerges as a potential therapeutic avenue for such cases. To shed light on the thalamo-cortical epileptogenic networks and refine prognostic indicators and treatments, we conducted an exhaustive examination of interictal data from thalamic stereoelectroencephalography (SEEG) recordings in a substantial patient cohort (n=121). Our investigation delved into thalamo-cortical connectivity, interictal hyperexcitability biomarkers, and their associations with clinical parameters during both rest and non-rapid eye movement (NREM) sleep states. Methodology: We conducted an observational study retrospectively gathering data from patients who underwent stereotactic-EEG with thalamic implantation as part of pre-surgical evaluation. Interictal recordings during rest and NREM sleep were analyzed to detect spikes and fast ripples automatically. Functional connectivity between the thalamus and other brain regions (involved or non-involved in the epileptogenic network) was examined using linear regression analysis (R2), while statistical evaluations assessed relationships between these measures, patient outcomes, and clinical variables. Results: Elevated rates of thalamic spikes and fast ripples during sleep were linked to unfavorable surgical outcomes (Engel class III/IV) compared to favorable outcomes (Engel class I/II). Thalamo-cortical functional connectivity analysis revealed heightened thalamic strength, particularly in the beta and gamma bands during sleep, among patients with poor surgical outcomes, especially with non-involved networks. Conversely, during rest, lower spike and fast ripple rates were observed in patients with longer epilepsy durations. Furthermore, thalamic strength values during resting state were diminished in patients with prolonged epilepsy durations and older age. Discussion: Our study uncovered heightened thalamic interictal activity and thalamo-cortical functional connectivity during sleep in patients with unfavorable surgical outcomes, within the largest cohort of patients with thalamic recordings documented. These findings inform pre-surgical assessments, aiding in identifying patients unsuitable for surgery and suggesting alternative interventions like DBS. Additionally, diminished thalamic activity and connectivity associated with epilepsy duration and age prompt speculation on the role of the thalamus as a pivotal hub in aging-related processes. Vigilance state-dependent insights from the thalamus underscore the necessity for comprehensive analyses to tailor stimulation protocols, facilitating a personalized therapeutic approach.

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The anterior and pulvinar thalamic nuclei interactions in mesial temporal lobe seizure networks

Cited by 13 publications

References 27 publications

Mapping hippocampal and thalamic atrophy in epilepsy: A 7‐T magnetic resonance imaging study

Mapping hippocampal and thalamic atrophy in epilepsy: A 7‐T magnetic resonance imaging study

Stereo‐EEG–based ictal functional connectivity in patients with periventricular nodular heterotopia–related epilepsy

Interictal waking and sleep electrophysiological properties of the thalamus in focal epilepsies

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