F Mauguière

Lyon Neuroscience Research Center, Lyons, Rhône-Alpes, France

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Publications (374)1159.15 Total impact

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    ABSTRACT: To explore whether painful somatosensory seizures (PSS) are generated in the primary somatosensory cortex (SI area) or in the operculo-insular cortex. We analyzed ictal recordings and data from stimulation using intracerebral electrodes exploring the operculo-insular cortex (including secondary somatosensory [SII] region), SI area, and other areas of the pain matrix (cingulate gyrus and supplementary motor area) in a case series study of 5 patients with PSS. Clinical features of PSS were different from those of seizures arising from the SI area: (1) pain intensity was higher; (2) pain spreading was not from one somatotopic territory to adjacent ones; and (3) the spatial extent of pain was large, fitting better with the size of somatosensory receptive fields of the insula and SII region than of the SI area. The insula and SII region were systematically involved at the onset of seizures, rapidly followed by the opercular portion of SI area. The upper part of SI cortex was involved at a lesser degree, with some delay, and pain duration did not correlate in time with that of the discharge in SI. Ictal pain was consistently reproduced by stimulation of the insula or SII region but never by stimulating the SI area. These data strongly suggest that PSS originate in the operculo-insular cortex and not in the SI area and corroborate the concept that this region is involved in the sensory-discriminative processing of pain inputs. Pain at the onset of PSS has a high value for localizing the epileptogenic area. © 2015 American Academy of Neurology.
    Neurology 01/2015; 84(6). · 8.30 Impact Factor
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    ABSTRACT: We have previously shown that an imaging marker, increased periventricular [11C]flumazenil ([11C]FMZ) binding, is associated with failure to become seizure free (SF) after surgery for temporal lobe epilepsy (TLE) with hippocampal sclerosis (HS). Here, we investigated whether increased preoperative periventricular white matter (WM) signal can be detected on clinical [18F]FDG-PET images. We then explored the potential of periventricular FDG WM increases, as well as whole-brain [11C]FMZ and [18F]FDG images analysed with random forest classifiers, for predicting surgery outcome.Methods Sixteen patients with MRI-defined HS had preoperative [18F]FDG and [11C]FMZ-PET. Fifty controls had [18F]FDG-PET (30), [11C]FMZ-PET (41), or both (21). Periventricular WM signal was analysed using Statistical Parametric Mapping (SPM8), and whole-brain image classification was performed using random forests implemented in R (http://www.r-project.org). Surgery outcome was predicted at the group and individual levels.ResultsAt the group level, non-seizure free (NSF) versus SF patients had periventricular increases with both tracers. Against controls, NSF patients showed more prominent periventricular [11C]FMZ and [18F]FDG signal increases than SF patients. All differences were more marked for [11C]FMZ. For individuals, periventricular WM signal increases were seen at optimized thresholds in 5/8 NSF patients for both tracers. For SF patients, 1/8 showed periventricular signal increases for [11C]FMZ, and 4/8 for [18F]FDG. Hence, [18F]FDG had relatively poor sensitivity and specificity. Random forest classification accurately identified 7/8 SF and 7/8 NSF patients using [11C]FMZ images, but only 4/8 SF and 6/8 NSF patients with [18F]FDG.Conclusion This study extends the association between periventricular WM increases and NSF outcome to clinical [18F]FDG-PET, but only at the group level. Whole-brain random forest classification increases [11C]FMZ-PET’s performance for predicting surgery outcome.
    NeuroImage: Clinical. 11/2014;
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    ABSTRACT: Objective: The present study provides a functional mapping of vestibular responses in the human insular cortex.Methods: 642 electrical stimulations of the insula were performed in 219 patients, using stereotactically implanted depth electrodes, during the pre-surgical evaluation of drug refractory partial epilepsy. We retrospectively identified 41 contacts where stimulation elicited vestibular sensations (VS) and analyzed their location with respect to (1) their stereotactic coordinates (for all contacts), (2) the anatomy of insula gyri (for 20 vestibular sites) and (3) the probabilistic cytoarchitectonic maps of the insula (for 9 vestibular sites).Results: VS occurred in 7.6% of the 541 evoked sensations after electrical stimulations of the insula. VS were mostly obtained after stimulation of the posterior insula, i.e. in the granular insular cortex and the postcentral insular gyrus. The data also suggest a spatial segregation of the responses in the insula, with the rotatory and translational VS being evoked at more posterior stimulation sites than other less definable VS. No left-right differences were observed.Interpretation: These results demonstrate vestibular sensory processing in the insula that is centered on its posterior part. The present data add to the understanding of the multiple sensory functions of the insular cortex and of the cortical processing of vestibular signals. It also indicates that lesion or dysfunction in the posterior insula should be considered during the evaluation of vestibular epileptic seizures. ANN NEUROL 2014. © 2014 American Neurological Association
    Annals of Neurology 08/2014; 76(4). · 11.91 Impact Factor
  • Maud Frot, Isabelle Faillenot, François Mauguière
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    ABSTRACT: Previous brain imaging studies have shown robust activations in the insula during nociceptive stimulation. Most activations involve the posterior insular cortex but they can cover all insular gyri in some fMRI studies. However, little is known about the timing of activations across the different insular sub-regions. We report on the distribution of intracerebrally recorded nociceptive laser evoked potentials (LEPs) acquired from the full extent of the insula in 44 epileptic patients. Our study shows that both posterior and anterior subdivisions of the insular cortex respond to a nociceptive heat stimulus within a 200-400 ms latency range. This nociceptive cortical potential occurs firstly, and is larger, in the posterior granular insular cortex. The presence of phase reversals in LEP components in both posterior and anterior insular regions suggests activation of distinct, presumably functionally separate, sources in the posterior and anterior parts of the insula. Our results suggest that nociceptive input is first processed in the posterior insula, where it is known to be coded in terms of intensity and anatomical location, and then conveyed to the anterior insula, where the emotional reaction to pain is elaborated. Hum Brain Mapp, 2014. © 2014 Wiley Periodicals, Inc.
    Human Brain Mapping 06/2014; · 6.92 Impact Factor
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    ABSTRACT: Transcranial electric stimulation elicited muscle motor evoked potentials (TESmMEPs) is one of the best methods for corticospinal tract's function monitoring during spine and spinal cord surgeries. A train of multipulse electric stimulation is required for eliciting TESmMEPs under general anaesthesia. Here, we investigated the best stimulation parameters for eliciting and recording tibialis anterior's TESmMEPs during paediatric scoliosis surgery. Numbers of pulses (NOP), inter-stimulus intervals (ISI) and current intensities allowing the best size tibialis anterior muscle's TESmMEPs under general anaesthesia, were tested and collected during 77 paediatric scoliosis surgery monitoring procedures in our hospital. Individual pulse duration was kept at 0.5ms and stimulating electrodes were positioned at C1 and C2 (International 10-20-EEG-System) during all the tests. The NOP used for eliciting the best tibialis anterior TESmMEPs response was 5, 6, and 7 respectively in 21 (27%), 47 (61%) and 9 (12%) out of the 77 patients. The ISI was 2, 3 and 4 ms respectively in 13 (17%), 55 (71%) and 9 (12%) of them. The current intensity used varied from 300 to 700V (mean: 448±136 V). Most patients had 6 as best NOP (61%) and 3ms as best ISI (71%). These findings support that a NOP of 6 and an ISI of 3 ms should be preferentially used as optimal stimulation settings for intraoperative tibialis anterior muscle's TESmMEPs eliciting and recording during paediatric scoliosis surgery.
    Neurophysiologie Clinique/Clinical Neurophysiology 10/2013; 43(4):243-250. · 1.46 Impact Factor
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    International journal of cardiology 09/2013; · 6.18 Impact Factor
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    ABSTRACT: Surgical treatment of epilepsy is a challenge for patients with non-contributive brain magnetic resonance imaging. However, surgery is feasible if the seizure-onset zone is precisely delineated through intracranial electroencephalography recording. We recently described a method, volumetric imaging of epileptic spikes, to delineate the spiking volume of patients with focal epilepsy using magnetoencephalography. We postulated that the extent of the spiking volume delineated with volumetric imaging of epileptic spikes could predict the localizability of the seizure-onset zone by intracranial electroencephalography investigation and outcome of surgical treatment. Twenty-one patients with non-contributive magnetic resonance imaging findings were included. All patients underwent intracerebral electroencephalography investigation through stereotactically implanted depth electrodes (stereo-electroencephalography) and magnetoencephalography with delineation of the spiking volume using volumetric imaging of epileptic spikes. We evaluated the spatial congruence between the spiking volume determined by magnetoencephalography and the localization of the seizure-onset zone determined by stereo-electroencephalography. We also evaluated the outcome of stereo-electroencephalography and surgical treatment according to the extent of the spiking volume (focal, lateralized but non-focal or non-lateralized). For all patients, we found a spatial overlap between the seizure-onset zone and the spiking volume. For patients with a focal spiking volume, the seizure-onset zone defined by stereo-electroencephalography was clearly localized in all cases and most patients (6/7, 86%) had a good surgical outcome. Conversely, stereo-electroencephalography failed to delineate a seizure-onset zone in 57% of patients with a lateralized spiking volume, and in the two patients with bilateral spiking volume. Four of the 12 patients with non-focal spiking volumes were operated upon, none became seizure-free. As a whole, patients having focal magnetoencephalography results with volumetric imaging of epileptic spikes are good surgical candidates and the implantation strategy should incorporate volumetric imaging of epileptic spikes results. On the contrary, patients with non-focal magnetoencephalography results are less likely to have a localized seizure-onset zone and stereo electroencephalography is not advised unless clear localizing information is provided by other presurgical investigation methods.
    Brain 09/2013; · 10.23 Impact Factor
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    ABSTRACT: IntroductionNeurophysiological studies point to altered cortical neuronal excitability in migraine patients.State of artBetween attacks, migraine brain seems to be “hyperresponsive” to repetitive stimuli, as suggested by evoked potential studies that show a lack of habituation to sensory stimuli. Transcranial magnetic stimulation suggests an impairment of intracortical inhibitory circuits in migraine, especially in migraine with aura. Controversial results are obtained in migraineurs without aura. Repetitive transcranial magnetic stimulation also shows in migraine with aura a paradoxical enhancement of intracortical facilitation by low frequency stimulation and greater increased facilitatory mechanisms by high-frequency stimulation. Importantly, cortical excitability level fluctuates over time in relation to the migraine cycle. The interictal lack of habituation to sensory stimuli normalizes before and during a migraine attack. Changes of cortical excitability consistent with the theory of cortical spreading depression are also observed during migraine aura with magnetoencephalography.PerspectivesThe exact role of cortical excitability changes in migraine pathophysiology and possibly in chronic migraine is still unknown. Further studies are also necessary to clarify the role of migraine preventive drugs on brain excitability.Conclusions In this review, the results of neurophysiological studies conducted in migraine patients will be described and the associated pathophysiological hypotheses will be discussed.
    Revue Neurologique 05/2013; 169(5):427–435. · 0.60 Impact Factor
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    ABSTRACT: PURPOSE: Mesio-temporal ictal semiology is sometimes observed in patients with large multilobar lesion. In this situation, surgery is often discarded because of the lesion size and/or suspicion of extended or multifocal epileptogenic areas. In this retrospective study we evaluated the surgical outcome of such patients in order to assess whether the electro-clinical presentation of seizures could be a prognostic marker of surgical outcome. METHODS: Among the temporal lobe epilepsy population explored in our department between 2000 and 2011 (240 patients), we identified 7 patients who presented an extensive lesion on brain Magnetic Resonance Imaging (MRI) (multilobar in four, hemispheric in two, and bilateral in one). All patients underwent (18)Fluorodeoxyglucose Positron Emission Tomography, which showed large, hemispheric or multilobar, areas of glucose hypometabolism. Because of the large lesion size, all patients were explored by stereoelectroencephalography (SEEG) before taking a decision regarding surgical indication. RESULTS: SEEG confirmed the temporal origin of the seizures and discarded the possibility of multiple epileptogenic zones. A temporal lobectomy, tailored on the basis of SEEG data, was proposed to the seven patients. The seven patients are classified Engel class I after the surgery (mean follow-up: 37.4±22.1 months). CONCLUSION: Our data thus suggest that, even in the absence of hippocampal MRI abnormality, ictal symptoms compatible with a temporal origin of seizures should be considered as a reliable indicator for surgery eligibility regardless of MRI lesion size. On the basis of our findings, the mesio-temporal semiology of seizures appears as one of the most reliable markers of operability in patients with large MRI lesions. These patients should not be excluded a priori from invasive exploration and surgical treatment, even if a large portion of their lesion is likely to be left in place after surgery.
    Seizure 03/2013; · 2.06 Impact Factor
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    ABSTRACT: A third of patients with intractable temporal lobe epilepsy and hippocampal sclerosis (HS) are not seizure free (NSF) after surgery. Increased periventricular [(11)C]flumazenil (FMZ) binding, reflecting heterotopic neuron concentration, has been described as one predictor of NSF outcome at the group level. We aimed to replicate this finding in an independent larger cohort and investigated whether NSF outcome can be predicted in individuals. Preoperative [(11)C]FMZ summed radioactivity images were available for 16 patients with HS and 41 controls. Images were analyzed using SPM8, explicitly including the white matter, and correction for global radioactivity via group-specific ANCOVA. Periventricular increases were assessed with a mask and different cutoffs for distinguishing NSF and seizure free (SF) patients. NSF patients had increased [(11)C]FMZ binding around the posterior horn of the ventricles ipsilaterally (z = 2.53) and contralaterally (z = 4.44) to the seizure focus compared with SF patients. Compared with controls, SF patients had fewer periventricular increases (two clusters, total volume 0.87 cm(3), zmax = 3.8) than NSF patients (two ipsilateral and three contralateral clusters, 6.15 cm(3), zmax = 4.8). In individuals and at optimized cutoffs, five (63%) of eight NSF patients and one (13%) of eight SF patients showed periventricular increases compared with controls (accuracy 75%). Only one (2%) of the 41 controls had increases at the same cutoff. The association between periventricular [(11)C]FMZ increases and NSF outcome after temporal lobe resection for HS has been confirmed in an independent cohort on simple summed activity images. [(11)C]FMZ-PET may be useful for individual preoperative counseling with clinically relevant accuracy.
    NeuroImage. Clinical. 01/2013; 3:242-248.
  • Perrine Devic, Philippe Petiot, François Mauguière
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    ABSTRACT: Introduction: Distal hereditary motor neuropathy (dHMN) is characterized by isolated distal muscle atrophy without sensory deficit. Nevertheless, clinical sensory loss has been reported despite preserved sensory nerve conduction in a few patients, thus differentiating these cases from the classical type 2 Charcot-Marie-Tooth disease (CMT2). Methods: We report 4 patients who presented with clinical sensory and motor neuropathy and normal peripheral sensory nerve conduction studies and were investigated with complete electrophysiological studies, including somatosensory evoked potentials (SEP). Results: These patients had a clinical presentation of classical CMT with isolated axonal motor neuropathy suggestive of dHMN. Interestingly, tibial nerve SEPs showed abnormalities suggestive of proximal involvement of dorsal roots that may explain the clinical somatosensory disturbances. Conclusions: These cases support the concept of spinal CMT that should be recognized as an intermediate form between dHMN and CMT2. SEP recording was helpful in defining a more precise phenotype of spinal CMT. Muscle Nerve 46: 603-607, 2012.
    Muscle & Nerve 10/2012; 46(4):604-9. · 2.31 Impact Factor
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    ABSTRACT: The feeling of being excluded from a social interaction triggers social pain, a sensation as intense as actual physical pain. Little is known about the neurophysiological underpinnings of social pain. We addressed this issue using intracranial electroencephalography in 15 patients performing a ball game where inclusion and exclusion blocks were alternated. Time-frequency analyses showed an increase in power of theta-band oscillations during exclusion in the anterior insula (AI) and posterior insula, the subgenual anterior cingulate cortex (sACC), and the fusiform "face area" (FFA). Interestingly, the AI showed an initial fast response to exclusion but the signal rapidly faded out. Activity in the sACC gradually increased and remained significant thereafter. This suggests that the AI may signal social pain by detecting emotional distress caused by the exclusion, whereas the sACC may be linked to the learning aspects of social pain. Theta activity in the FFA was time-locked to the observation of a player poised to exclude the participant, suggesting that the FFA encodes the social value of faces. Taken together, our findings suggest that theta activity represents the neural signature of social pain. The time course of this signal varies across regions important for processing emotional features linked to social information.
    Cerebral Cortex 08/2012; · 8.31 Impact Factor
  • Maud Frot, Michel Magnin, François Mauguière, Luis Garcia-Larrea
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    ABSTRACT: Intracortical evoked potentials to nonnoxious Aβ (electrical) and noxious Aδ (laser) stimuli within the human primary somatosensory (S1) and motor (M1) areas were recorded from 71 electrode sites in 9 epileptic patients. All cortical sites responding to specific noxious inputs also responded to nonnoxious stimuli, while the reverse was not always true. Evoked responses in S1 area 3b were systematic for nonnoxious inputs, but seen in only half of cases after nociceptive stimulation. Nociceptive responses were systematically recorded when electrode tracks reached the crown of the postcentral gyrus, consistent with an origin in somatosensory areas 1-2. Sites in the precentral cortex also exhibited noxious and nonnoxious responses with phase reversals indicating a local origin in area 4 (M1). We conclude that a representation of thermal nociceptive information does exist in human S1, although to a much lesser extent than the nonnociceptive one. Notably, area 3b, which responds massively to nonnoxious Aβ activation was less involved in the processing of noxious heat. S1 and M1 responses to noxious heat occurred at latencies comparable to those observed in the supra-sylvian opercular region of the same patients, suggesting a parallel, rather than hierarchical, processing of noxious inputs in S1, M1 and opercular cortex. This study provides the first direct evidence for a spinothalamic related input to the motor cortex in humans. Hum Brain Mapp, 2012. © 2012 Wiley Periodicals, Inc.
    Human Brain Mapping 06/2012; · 6.92 Impact Factor
  • Neurophysiologie Clinique/Clinical Neurophysiology 04/2012; 42(3):164. · 1.46 Impact Factor
  • Revue Neurologique 04/2012; 168:A90-A91. · 0.60 Impact Factor
  • Sleep Medicine 03/2012; 13(5):554-6. · 3.10 Impact Factor
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    ABSTRACT: The role of operculo-insular region in the processing of somato-sensory inputs, painful or not, is now well established. However, available maps from previous literature show a substantial overlap of cortical areas activated by these stimuli, and the region referred to as the "secondary somatosensory area (SII)" is widely distributed in the parietal operculum. Differentiating SII from posterior insula cortex, which is anatomically contiguous, is not easy, explaining why the "operculo-insular" label has been introduced to describe activations by somatosensory stimuli in this cortical region. Based on the recent cyto-architectural parcellation of the human insular/SII cortices (Eickhoff et al., 2006, Kurth et al., 2010), the present study investigates with functional MRI (fMRI), whether these structural subdivisions could subserve distinct aspects of discriminative somato-sensory functions, including pain. Responses to five types of stimuli applied on the left hand of 25 healthy volunteers were considered: i) tactile stimuli; ii) passive movements; iii) innocuous cold stimuli; iv) non-noxious warm and v) heat pain. Our results show different patterns of activation depending on the type of somato-sensory stimulation. The posterior part of SII (OP1 area), contralateral to stimuli, was the only sub-region activated by all type of stimuli and might therefore be considered as a common cortical target for different types of somato-sensory inputs. Proprioceptive stimulation by passive finger movements activated the posterior part of SII (OP1 sub-region) bilaterally and the contralateral median part of insula (PreCG and MSG). Innocuous cooling activated the contralateral posterior part of SII (OP1) and the dorsal posterior and median part of insula (OP2, PostCG). Pain stimuli induced the most widespread and intense activation that was bilateral in SII (OP1, OP4) and distributed to all sub-regions of contralateral insula (except OP2) and to the anterior part of the ipsilateral insula (PreCG, MSG, ASG). However, the posterior granular part of insula contralateral to stimulus (Ig area) and the anterior part of SII bilaterally (OP4) were specifically activated during pain stimulation. This raises the question whether these latter areas could be the anatomical substrate of the sensory-discriminative processing of thermal pain.
    NeuroImage 03/2012; 60(1):409-18. · 6.13 Impact Factor
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    ABSTRACT: Interictal spikes are a hallmark of cortical epileptogenicity; their spatial distribution in the cortex defines the so-called 'irritative' zone or spiking volume (SV). Delineating the SV precisely is a challenge during the presurgical evaluation of patients with epilepsy. Magnetoencephalography (MEG) recordings enable determination of the brain sources of epileptic spikes using source localization procedures. Most previous clinical MEG studies have relied on dipole modeling of epileptic spikes, which does not permit a volumetric estimation of the spiking cortex. In the present study, we propose a new source modeling procedure, Volumetric Imaging of Epileptic Spikes (VIES). In VIES, the SV is identified as the 3D region where sources of the high frequency activities (>20 Hz) associated with epileptic spikes are distributed. We localized these sources using a beamforming approach (DICS, Dynamic Imaging of Coherent Neural Sources). To determine the optimal parameters and accuracy of the method, we compared the SV obtained by VIES with the SV defined by the invasive gold standard, intracranial stereotactic EEG recordings (SEEG), in 21 patients with focal epilepsy. Using rigorous validation criteria based on the exact anatomical location of SEEG contacts, we found that the overall sensitivity of VIES for detecting spiking SEEG contacts was 76% and its specificity for correctly identifying non-spiking SEEG contacts was 67%, indicating a good agreement between VIES and SEEG. Moreover, we found that classical dipole clustering was not informative in 9/21 patients, while VIES enable to delineate the SV in all patients. For the 12 patients having a SV delineated both with VIES and dipole clustering, VIES method had higher sensitivity and lower specificity. This proof-of-concept study shows that VIES is a promising approach to non-invasive estimation of the SV in focal epilepsy.
    NeuroImage 02/2012; 59(4):3955-66. · 6.13 Impact Factor
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    Laure Mazzola, Jean Isnard, Roland Peyron, François Mauguière
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    ABSTRACT: Thanks to the seminal work of Wilder Graves Penfield (1891-1976) at the Montreal Neurological Institute, electrical stimulation is used worldwide to localize the epileptogenic cortex and to map the functionally eloquent areas in the context of epilepsy surgery or lesion resections. In the functional map of elementary and experiential responses he described through >20 years of careful exploration of the human cortex via stimulation of the cortical surface, Penfield did not identify any 'pain cortical area'. We reinvestigated this issue by analysing subjective and videotaped behavioural responses to 4160 cortical stimulations using intracerebral electrodes implanted in all cortical lobes that were carried out over 12 years during the presurgical evaluation of epilepsy in 164 consecutive patients. Pain responses were scarce (1.4%) and concentrated in the medial part of the parietal operculum and neighbouring posterior insula where pain thresholds showed a rostrocaudal decrement. This deep cortical region remained largely inaccessible to the intraoperative stimulation of the cortical surface carried out by Penfield after resection of the parietal operculum. It differs also from primary sensory areas described by Penfield et al. in the sense that, with our stimulation paradigm, pain represented only 10% of responses. Like Penfield et al., we obtained no pain response anywhere else in the cortex, including in regions consistently activated by pain in most functional imaging studies, i.e. the first somatosensory area, the lateral part of the secondary somatosensory area, anterior and mid-cingulate gyri (mid-cingulate cortex), anterior frontal, posterior parietal and supplementary motor areas. The medial parietal operculum and posterior insula are thus the only areas where electrical stimulation is able to trigger activation of the pain cortical network and thus the experience of somatic pain.
    Brain 02/2012; 135(Pt 2):631-40. · 10.23 Impact Factor

Publication Stats

10k Citations
1,159.15 Total Impact Points

Institutions

  • 2010–2014
    • Lyon Neuroscience Research Center
      Lyons, Rhône-Alpes, France
  • 1995–2014
    • Claude Bernard University Lyon 1
      • Faculté de pharmacie - Institut des sciences pharmaceutiques et biologiques (ISPB)
      Villeurbanne, Rhône-Alpes, France
  • 2013
    • Cancer Research Center of Lyon
      Lyons, Rhône-Alpes, France
  • 2006–2013
    • Hospices Civils de Lyon
      Lyons, Rhône-Alpes, France
  • 1989–2012
    • University of Lyon
      Lyons, Rhône-Alpes, France
  • 1990–2011
    • CHU de Lyon - Hôpital Neurologique et Neurochirurgical Pierre Wertheimer
      Lyons, Rhône-Alpes, France
    • Centre Hospitalier Universitaire de Saint-Étienne
      • Department of Neurology
      Saint-Étienne, Rhône-Alpes, France
  • 1986–2011
    • Unité Inserm U1077
      Caen, Lower Normandy, France
  • 2007–2010
    • French Institute of Health and Medical Research
      Lutetia Parisorum, Île-de-France, France
  • 1999–2008
    • University Joseph Fourier - Grenoble 1
      • Centre d'Investigation Clinique
      Grenoble, Rhône-Alpes, France
  • 2005
    • University of Malaga
      • Area of Physiology
      Málaga, Andalusia, Spain
  • 2004
    • The Neurosciences Institute
      La Jolla, California, United States
  • 1992–2004
    • CERMEP
      Rhône-Alpes, France
  • 1992–2002
    • The Catholic University of America
      Washington, Washington, D.C., United States
  • 1994–2000
    • Catholic University of the Sacred Heart
      • Institute of Neurology
      Roma, Latium, Italy
  • 1996
    • Faculté des Sciences Ain Chock - Casablanca
      Anfa, Grand Casablanca, Morocco
    • University of Helsinki
      • Cognitive Brain Research Unit
      Helsinki, Province of Southern Finland, Finland