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January 12, 2021; 96 (2) Article

The Ictal Signature of Thalamus and Basal Ganglia in Focal Epilepsy

A SEEG Study

View ORCID ProfileFrancesca Pizzo, View ORCID ProfileNicolas Roehri, View ORCID ProfileBernard Giusiano, View ORCID ProfileStanislas Lagarde, View ORCID ProfileRomain Carron, View ORCID ProfileDidier Scavarda, View ORCID ProfileAileen McGonigal, Cristina Filipescu, View ORCID ProfileIsabelle Lambert, View ORCID ProfileFrancesca Bonini, View ORCID ProfileAgnes Trebuchon, View ORCID ProfileChristian-George Bénar, View ORCID ProfileFabrice Bartolomei
First published October 6, 2020, DOI: https://doi.org/10.1212/WNL.0000000000011003
Francesca Pizzo
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Nicolas Roehri
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Bernard Giusiano
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Stanislas Lagarde
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Romain Carron
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Didier Scavarda
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Aileen McGonigal
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Cristina Filipescu
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Isabelle Lambert
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Francesca Bonini
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Agnes Trebuchon
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Christian-George Bénar
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Fabrice Bartolomei
From the Epileptology Department (F.P., S.L., A.M., I.L., F. Bonini, A.T., F. Bartolomei), Functional and Stereotactic Neurosurgery (R.C.), and Pediatric Neurosurgery (D.S.), APHM, Timone Hospital, Institut de Neurosciences des Systèmes (F.P., N.R., B.G., S.L., R.C., D.S., A.M., I.L., F. Bonini, A.T., C.-G.B, F. Bartolomei), INSERM, Aix Marseille Universite; and Psychiatrie et Neurosciences (C.F.), GHU Paris, St Anne, Paris.
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Citation
The Ictal Signature of Thalamus and Basal Ganglia in Focal Epilepsy
A SEEG Study
Francesca Pizzo, Nicolas Roehri, Bernard Giusiano, Stanislas Lagarde, Romain Carron, Didier Scavarda, Aileen McGonigal, Cristina Filipescu, Isabelle Lambert, Francesca Bonini, Agnes Trebuchon, Christian-George Bénar, Fabrice Bartolomei
Neurology Jan 2021, 96 (2) e280-e293; DOI: 10.1212/WNL.0000000000011003

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Abstract

Objective To determine the involvement of subcortical regions in human epilepsy by analyzing direct recordings from these regions during epileptic seizures using stereo-EEG (SEEG).

Methods We studied the SEEG recordings of a large series of patients (74 patients, 157 seizures) with an electrode sampling the thalamus and in some cases also the basal ganglia (caudate nucleus, 22 patients; and putamen, 4 patients). We applied visual analysis and signal quantification methods (Epileptogenicity Index [EI]) to their ictal recordings and compared electrophysiologic with clinical data.

Results We found that in 86% of patients, thalamus was involved during seizures (visual analysis) and 20% showed high values of epileptogenicity (EI >0.3). Basal ganglia may also disclose high values of epileptogenicity (9% in caudate nucleus) but to a lesser degree than thalamus (p < 0.01). We observed different seizure onset patterns including low voltage high frequency activities. We found high values of thalamic epileptogenicity in different epilepsy localizations, including opercular and motor epilepsies. We found no difference between epilepsy etiologies (cryptogenic vs malformation of cortical development, p = 0.77). Thalamic epileptogenicity was correlated with the extension of epileptogenic networks (p = 0.02, ρ 0.32). We found a significant effect (p < 0.05) of thalamic epileptogenicity regarding the postsurgical outcome (higher thalamic EI corresponding to higher probability of surgical failure).

Conclusions Thalamic involvement during seizures is common in different seizure types. The degree of thalamic epileptogenicity is a possible marker of the epileptogenic network extension and of postsurgical prognosis.

Glossary

CI=
confidence interval;
DBS=
deep brain stimulation;
EI=
Epileptogenicity Index;
EZ=
epileptogenic zone;
LVFA=
low voltage fast activity;
MCD=
malformation of cortical development;
MTLE=
mesiotemporal lobe epilepsy;
nTF=
normalized time frequency;
PT=
planum temporale;
RS=
rhythmic spikes;
SEEG=
stereo-EEG;
SOP=
seizure onset pattern;
TLE=
temporal lobe epilepsy

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • ↵* These authors contributed equally to this work.

  • CME Course: NPub.org/cmelist

  • Received January 30, 2020.
  • Accepted in final form August 26, 2020.
  • © 2020 American Academy of Neurology
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