The role of the dorsal anterior insula in ecstatic sensation revealed by direct electrical brain stimulation.


Journal

Brain stimulation
ISSN: 1876-4754
Titre abrégé: Brain Stimul
Pays: United States
ID NLM: 101465726

Informations de publication

Date de publication:
Historique:
received: 16 02 2019
revised: 13 05 2019
accepted: 03 06 2019
pubmed: 15 6 2019
medline: 14 1 2020
entrez: 15 6 2019
Statut: ppublish

Résumé

An ecstatic phenomenon is an altered state of consciousness with a sense of "hyper-reality", and a complete present-moment awareness with a feeling of union with the Universe. A better understanding of the network mechanisms underlying this fascinating subjective experience may help to unravel some mysteries of human consciousness. Insula has been recently proposed to be a key region to elicit these symptoms. We studied functional connectivity changes in several brain areas during the induction of ecstatic auras by direct electrical stimulation of the dorsal anterior insular cortex in patients with refractory focal epilepsy implanted with intracerebral electrodes (stereotactic-EEG, SEEG) in the context of their pre-surgical evaluation. Three patients were selected on the basis of the occurrence of ecstatic symptoms triggered by direct intracerebral electrical stimulation (ES) of the antero-dorsal part of the insula. ES was performed (50 Hz, 1.5-2.1 mA, in a bipolar fashion to each contact in the gray matter during a 3 s period) to map functional cortices and trigger habitual seizures. One stimulation inducing ecstatic changes in each patient was analyzed. Functional connectivity analysis was performed by measuring interdependencies (nonlinear regression analysis based on the h In all patients, only the stimulation of dorsal anterior insula was able to reproduce an ecstatic aura. We observed a significant increase of functional connectivity values between several brain regions in the immediate period following stimulations. The most commonly implicated region was the dorsal anterior insula. Out-degrees (a measure intended to identify leading structures in a network) identified the dorsal anterior insula as the most common leading region in the induced networks. Our findings bring additional support in favor of a major role played by the dorsal anterior insula in ecstatic experiences.

Sections du résumé

BACKGROUND
An ecstatic phenomenon is an altered state of consciousness with a sense of "hyper-reality", and a complete present-moment awareness with a feeling of union with the Universe. A better understanding of the network mechanisms underlying this fascinating subjective experience may help to unravel some mysteries of human consciousness. Insula has been recently proposed to be a key region to elicit these symptoms.
OBJECTIVE/HYPOTHESIS
We studied functional connectivity changes in several brain areas during the induction of ecstatic auras by direct electrical stimulation of the dorsal anterior insular cortex in patients with refractory focal epilepsy implanted with intracerebral electrodes (stereotactic-EEG, SEEG) in the context of their pre-surgical evaluation.
METHODS
Three patients were selected on the basis of the occurrence of ecstatic symptoms triggered by direct intracerebral electrical stimulation (ES) of the antero-dorsal part of the insula. ES was performed (50 Hz, 1.5-2.1 mA, in a bipolar fashion to each contact in the gray matter during a 3 s period) to map functional cortices and trigger habitual seizures. One stimulation inducing ecstatic changes in each patient was analyzed. Functional connectivity analysis was performed by measuring interdependencies (nonlinear regression analysis based on the h
RESULTS
In all patients, only the stimulation of dorsal anterior insula was able to reproduce an ecstatic aura. We observed a significant increase of functional connectivity values between several brain regions in the immediate period following stimulations. The most commonly implicated region was the dorsal anterior insula. Out-degrees (a measure intended to identify leading structures in a network) identified the dorsal anterior insula as the most common leading region in the induced networks.
CONCLUSION(S)
Our findings bring additional support in favor of a major role played by the dorsal anterior insula in ecstatic experiences.

Identifiants

pubmed: 31196836
pii: S1935-861X(19)30230-X
doi: 10.1016/j.brs.2019.06.005
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1121-1126

Informations de copyright

Copyright © 2019 Elsevier Inc. All rights reserved.

Auteurs

F Bartolomei (F)

Aix Marseille Univ, INSERM, INS, Inst Neurosci Syst, Marseille, France; APHM, Timone Hospital, Clinical Neurophysiology and Epileptology Department, Marseille, 13005, France. Electronic address: Fabrice.bartolomei@ap-hm.fr.

S Lagarde (S)

Aix Marseille Univ, INSERM, INS, Inst Neurosci Syst, Marseille, France; APHM, Timone Hospital, Clinical Neurophysiology and Epileptology Department, Marseille, 13005, France.

D Scavarda (D)

Aix Marseille Univ, INSERM, INS, Inst Neurosci Syst, Marseille, France; Department of Pediatric Neurosurgery, Timone University Hospital, Marseille, France.

R Carron (R)

Aix Marseille Univ, INSERM, INS, Inst Neurosci Syst, Marseille, France; Department of Functional and Stereotactic Neurosurgery, Timone University Hospital, Marseille, France.

C G Bénar (CG)

Aix Marseille Univ, INSERM, INS, Inst Neurosci Syst, Marseille, France.

F Picard (F)

Department of Neurology, University Hospitals and Medical School of Geneva, Geneva, Switzerland.

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Classifications MeSH