Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental study

Background: Although the mechanisms by which deep brain stimulation (DBS) modifies the activity of the ictal network are mostly undefined, recent studies have suggested that DBS of the anterior nucleus of the thalamus (ANT) can be an effective treatment for mesial temporal lobe epilepsy (MTLE) when...

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Main Authors: Ariana Sherdil, Stephan Chabardès, Olivier David, Brigitte Piallat
Format: Article
Language:English
Published: Elsevier 2020-11-01
Series:Brain Stimulation
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1935861X20302655
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spelling doaj-8ba9661990c048bbaab203477440fd8f2021-03-19T07:23:07ZengElsevierBrain Stimulation1935-861X2020-11-0113616781686Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental studyAriana Sherdil0Stephan Chabardès1Olivier David2Brigitte Piallat3Inserm, U1216, Grenoble, F-38000, France; Univ Grenoble Alpes, Grenoble, F-38000, FranceInserm, U1216, Grenoble, F-38000, France; Univ Grenoble Alpes, Grenoble, F-38000, France; CHU Grenoble Alpes, Department of Neurosurgery, Grenoble, F-38000, France; Clinatec, Research Centre Edmond Safra, CEA-LETI, Grenoble, F-38000, FranceInserm, U1216, Grenoble, F-38000, France; Univ Grenoble Alpes, Grenoble, F-38000, FranceInserm, U1216, Grenoble, F-38000, France; Univ Grenoble Alpes, Grenoble, F-38000, France; Corresponding author. Grenoble Institut des Neurosciences, Chemin Fortuné Ferrini – Bât EJ Safra – CHU, 38700, La Tronche, France.Background: Although the mechanisms by which deep brain stimulation (DBS) modifies the activity of the ictal network are mostly undefined, recent studies have suggested that DBS of the anterior nucleus of the thalamus (ANT) can be an effective treatment for mesial temporal lobe epilepsy (MTLE) when resective surgery cannot be performed. In a nonhuman primate (NHP) model of MTL seizures, we showed that the ANT was actively involved during interictal and ictal periods through different patterns and that the hippocampus (HPC) and ANT synchronously oscillate in the high beta-band during seizures. Objective: Based on those findings, we evaluated whether the frequency of stimulation is an important parameter that interferes with seizures and how to adapt stimulation protocols to it. Methods: We investigated the effects of low-frequency (40 Hz - determined as the ictal frequency of correlation between structures) and high-frequency (130 Hz - as commonly used in clinic) ANT stimulation in three monkeys in which MTLE seizures were initiated. Results: Low-frequency stimulation had a strong effect on the number of seizures and the total time spent in seizure, whereas high-frequency stimulation had no effect. The coherence of oscillations between the HPC and the ANT was significantly correlated with the success of low-frequency stimulation: the greater the coherence was, the greater the antiepileptic effect of ANT-DBS. Conclusion: Our results suggest that low-frequency stimulation is efficient in treating seizures in a nonhuman primate model. More importantly, the study of the coherence between the ANT and HPC during seizures can help to predict the anti-epileptic effects of ANT stimulation. Furthermore, the DBS paradigm could be customized in frequency for each patient on the basis of the coherence spectral pattern.http://www.sciencedirect.com/science/article/pii/S1935861X20302655Mesial temporal lobe epilepsyDeep brain stimulationOscillation coherenceNon-human primateAnterior thalamic nucleus
collection DOAJ
language English
format Article
sources DOAJ
author Ariana Sherdil
Stephan Chabardès
Olivier David
Brigitte Piallat
spellingShingle Ariana Sherdil
Stephan Chabardès
Olivier David
Brigitte Piallat
Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental study
Brain Stimulation
Mesial temporal lobe epilepsy
Deep brain stimulation
Oscillation coherence
Non-human primate
Anterior thalamic nucleus
author_facet Ariana Sherdil
Stephan Chabardès
Olivier David
Brigitte Piallat
author_sort Ariana Sherdil
title Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental study
title_short Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental study
title_full Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental study
title_fullStr Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental study
title_full_unstemmed Coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: An experimental study
title_sort coherence between the hippocampus and anterior thalamic nucleus as a tool to improve the effect of neurostimulation in temporal lobe epilepsy: an experimental study
publisher Elsevier
series Brain Stimulation
issn 1935-861X
publishDate 2020-11-01
description Background: Although the mechanisms by which deep brain stimulation (DBS) modifies the activity of the ictal network are mostly undefined, recent studies have suggested that DBS of the anterior nucleus of the thalamus (ANT) can be an effective treatment for mesial temporal lobe epilepsy (MTLE) when resective surgery cannot be performed. In a nonhuman primate (NHP) model of MTL seizures, we showed that the ANT was actively involved during interictal and ictal periods through different patterns and that the hippocampus (HPC) and ANT synchronously oscillate in the high beta-band during seizures. Objective: Based on those findings, we evaluated whether the frequency of stimulation is an important parameter that interferes with seizures and how to adapt stimulation protocols to it. Methods: We investigated the effects of low-frequency (40 Hz - determined as the ictal frequency of correlation between structures) and high-frequency (130 Hz - as commonly used in clinic) ANT stimulation in three monkeys in which MTLE seizures were initiated. Results: Low-frequency stimulation had a strong effect on the number of seizures and the total time spent in seizure, whereas high-frequency stimulation had no effect. The coherence of oscillations between the HPC and the ANT was significantly correlated with the success of low-frequency stimulation: the greater the coherence was, the greater the antiepileptic effect of ANT-DBS. Conclusion: Our results suggest that low-frequency stimulation is efficient in treating seizures in a nonhuman primate model. More importantly, the study of the coherence between the ANT and HPC during seizures can help to predict the anti-epileptic effects of ANT stimulation. Furthermore, the DBS paradigm could be customized in frequency for each patient on the basis of the coherence spectral pattern.
topic Mesial temporal lobe epilepsy
Deep brain stimulation
Oscillation coherence
Non-human primate
Anterior thalamic nucleus
url http://www.sciencedirect.com/science/article/pii/S1935861X20302655
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