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Role of Operculoinsular Cortices in Human Pain Processing: Converging Evidence from PET, fMRI, Dipole Modeling, and Intracerebral Recordings of Evoked Potentials

Peyron, R., Frot, M., Schneider, F., Garcia-Larrea, L., Mertens, P., Barral, F.G., Sindou, M., Laurent, B., Mauguière, F.·2002·NeuroImage

DOI 10.1006/nimg.2002.1315

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Abstract

Insular and SII cortices have been consistently shown by PET, fMRI, EPs, and MEG techniques to be activated bilaterally by a nociceptive stimulation. The aim of the present study was to refer to, and to compare within a common stereotactic space, the nociceptive responses obtained in humans by (i) PET, (ii) fMRI, (iii) dipole modeling of scalp LEPs, and (iv) intracerebral recordings of LEPs. PET, fMRI, and scalp LEPs were obtained from normal subjects during thermal pain. Operculoinsular LEPs were obtained from 13 patients using deep brain electrodes implanted for presurgical evaluation of drug-resistant epilepsy. Whatever the technique, we obtained responses which were located bilaterally in the insular and SII cortices. In electrophysiological responses (LEPs) the SII insular contribution peaked between 150 and 250 ms poststimulus and corresponded to the earliest portions of the whole cerebral response. Group analysis of PET and fMRI data showed highly consistent responses contralateral to stimulation. On single-subject analysis, LEPs and fMRI activations were concentrated in relatively restricted volumes even though spatial sampling was quite different for both techniques. Despite our multimodal approach, however, it was not possible to separate insular from SII activities. Individual variations in the anatomy and function of SII and insular cortices may explain this limitation. This multimodal study provides, however, cross-validated spatial and temporal information on the pain-related processes occurring in the operculoinsular region, which thus appears as a major site for the early cortical pain encoding in the human brain.

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Authors: Peyron, R., Frot, M., Schneider, F., Garcia-Larrea, L., Mertens, P., Barral, F. G., Sindou, M., Laurent, B., & Mauguière, F.
Affiliations: Lyon 1 Université (FR)
Corresponding author: Peyron, R.
ORCID: Peyron, R.
Frot, M.
Schneider, F.
Mertens, P.
Sindou, M.
Laurent, B.
Venue: NeuroImage
Publisher: Elsevier BV
Published: 2002-11
Volume: 17
Issue: 3
Pages: 1336-1346
ISSN: 1053-8119 (ISSN-L)
DOI: 10.1006/nimg.2002.1315
OpenAlex: W1989396758
Cited by: 209
References: 64
Citations by year: 2026: 1 · 2024: 4 · 2023: 5 · 2022: 3 · 2021: 4 · 2020: 7 · 2019: 11 · 2018: 4 · 2017: 4 · 2016: 7 · 2015: 7 · 2014: 3 · 2013: 11 · 2012: 6
FWCI: 8.59
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: NeuroImage (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Topics: Health Sciences › Medicine › Physiology (medical) › Pain Mechanisms and Treatments
Health Sciences › Medicine › Anesthesiology and Pain Medicine › Pain Management and Treatment
Life Sciences › Neuroscience › Cognitive Neuroscience › Pain Management and Placebo Effect
Keywords: pain processing, somatosensory cortex, insula, secondary somatosensory cortex, nociception, thermal pain, dipole modeling, intracerebral recordings, PET, functional MRI, multimodal neuroimaging, individual anatomical variation
MeSH terms: Adult, Brain Mapping, Cerebral Cortex, Dominance, Cerebral, Electrodes, Implanted, Electroencephalography, Epilepsy, Temporal Lobe, Female, Frontal Lobe, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Middle Aged, Synaptic Transmission, Nociceptors, Oxygen, Pain, Tomography, Emission-Computed, Pain Threshold

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Role of Operculoinsular Cortices in Human Pain Processing: Converging Evidence from PET, fMRI, Dipole Modeling, and Intracerebral Recordings of Evoked Potentials

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