Mapping the Insula with Stereo-Electroencephalography: The Emergence of Semiology in Insula Lobe Seizures.
Journal
Annals of neurology
ISSN: 1531-8249
Titre abrégé: Ann Neurol
Pays: United States
ID NLM: 7707449
Informations de publication
Date de publication:
09 2020
09 2020
Historique:
received:
15
03
2020
revised:
30
05
2020
accepted:
07
06
2020
pubmed:
17
6
2020
medline:
5
1
2021
entrez:
17
6
2020
Statut:
ppublish
Résumé
Insula epilepsy is rare and can be evaluated effectively by Stereotactic intracerebral EEG (SEEG). Many previous studies of insulo-opercular seizures have been unable to separate insular and opercular onset. With adequate sampling of the insula, this study shows this is possible. We analyzed intrainsular dynamics and extrainsular propagation in 12 patients with "pure" insula epilepsy (n = 9) or insular and only deepest opercular involvement (n = 3) at seizure onset. Review of semiology defined clinical groups, agglomerative cluster, and principal component analysis of semiological features were performed. Quantitative epileptogenicity, and intrainsular and extrainsular propagation were computed via time frequency analysis and epileptogenicity mapping. Seizure onset patterns were heterogeneous; the seizure onset zone was focal. Seizure onset and first ictal change within insula functional subdivision correlated with aura and reflex component. No paninsular spread occurred; contralateral insular spread was very early. While the discharge was intrainsular, clinical signs related to aura or vegetative signs. Extrainsular propagation was early and related to the emergence of the majority of clinical signs. Cluster analysis found an anterior, intermediate, and posterior insula seizure onset group. The largest principal component separated anterior insula manifestations, including early hypermotor signs, early recovery, and no aura from posterior insula features of early dystonia, early tonic motor features, and sensorimotor aura. Aura is vital to identifying seizure onset and relates to insula functional subdivision. Seizures are heterogenous; extrainsular propagation occurs early, accounting for most of the semiology. With adequate sampling, "pure" insula epilepsy can be identified and focal curative resection is possible. ANN NEUROL 2020;88:477-488.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
477-488Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2020 American Neurological Association.
Références
Morel A, Gallay MN, Baechler A, et al. The human insula: architectonic organization and postmortem MRI registration. Neuroscience 2013;236:117-135.
Mufson EJ, Mesulam MM, Pandya DN. Insular interconnections with the amygdala in the rhesus monkey. Neuroscience 1981;6:1231-1248.
Cerliani L, Thomas RM, Jbabdi S, et al. Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex. Hum Brain Mapp 2012;33:2005-2034.
Namkung H, Kim SH, Sawa A. The insula: an underestimated brain area in clinical neuroscience, psychiatry, and neurology. Trends Neurosci 2017;40:200-207.
Guillaume MMJ, Mazars G. Cinq cas de foyers épileptogènes insulaires opérés. Soc Française de Neurol 1949;766-769.
Kaada BR, Jasper H. Respiratory responses to stimulation of temporal pole, insula, and hippocampal and limbic gyri in man. AMA Arch Neurol Psychiatry 1952;68:609-619.
Silfvenius H, Gloor P, Rasmussen T. Evaluation of insular ablation in surgical treatment of temporal lobe epilepsy. Epilepsia 1964;5:307-320.
Duffau H, Capelle L, Lopes M, et al. Medically intractable epilepsy from insular low-grade gliomas: improvement after an extended lesionectomy. Acta Neurochir 2002;144:563-573.
Isnard J, Guenot M, Ostrowsky K, et al. The role of the insular cortex in temporal lobe epilepsy. Ann Neurol 2000;48:614-623.
Isnard J, Guénot M, Sindou M, Mauguière F. Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 2004;45:1079-1090.
Nguyen DK, Nguyen DB, Malak R, et al. Revisiting the role of the insula in refractory partial epilepsy. Epilepsia 2009;50:510-520.
Blauwblomme T, Kahane P, Minotti L, et al. Multimodal imaging reveals the role of gamma activity in eating-reflex seizures. J Neurol Neurosurg Psychiatry 2011;82:1171-1173.
Ryvlin P, Minotti L, Demarquay G, et al. Nocturnal hypermotor seizures, suggesting frontal lobe epilepsy, can originate in the insula. Epilepsia 2006;47:755-765.
Proserpio P, Cossu M, Francione S, et al. Insular-opercular seizures manifesting with sleep-related paroxysmal motor behaviors: a stereo-EEG study. Epilepsia 2011;52:1781-1791.
Hagiwara K, Jung J, Bouet R, et al. How can we explain the frontal presentation of insular lobe epilepsy? The impact of non-linear analysis of insular seizures. Clin Neurophysiol 2017;128:780-791.
Dylgjeri S, Taussig D, Chipaux M, et al. Insular and insulo-opercular epilepsy in childhood: an SEEG study. Seizure 2014;23:300-308.
Gras-Combe G, Minotti L, Hoffmann D, et al. Surgery for nontumoral insular epilepsy explored by stereoelectroencephalography. Neurosurgery 2016;79:578-588.
Abel TJ, Varela Osorio R, Amorim-Leite R, et al. Frameless robot-assisted stereoelectroencephalography in children: technical aspects and comparison with Talairach frame technique. J Neurosurg Pediatr 2018;22:37-46.
Deman P, Bhattacharjee M, Tadel F, et al. IntrAnat electrodes: a free database and visualization software for intracranial electroencephalographic data processed for case and group studies. Front Neuroinform 2018;12:40.
Kahane P, Tassi L, Francione S, et al. Manifestations électro-cliniques induites par la stimulation électrique intra-cérébrale par "chocs" dans les épilepsies temporales. Neurophysiol Clin 1993;22:305-326.
Lagarde S, Buzori S, Trebuchon A, et al. The repertoire of seizure onset patterns in human focal epilepsies: determinants and prognostic values. Epilepsia 2019;60:85-95.
David O, Blauwblomme T, Job AS, et al. Imaging the seizure onset zone with stereo-electroencephalography. Brain 2011;134:2898-2911.
Tadel F, Baillet S, Mosher JC, et al. Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011;2011:879716.
Job AS, David O, Minotti L, et al. Epileptogenicity maps of intracerebral fast activities (60-100 Hz) at seizure onset in epilepsy surgery candidates. Front Neurol 2019;10:1263.
Grinenko O, Li J, Mosher JC, et al. A fingerprint of the epileptogenic zone in human epilepsies. Brain 2018;141:117-131.
Kurth F, Zilles K, Fox PT, et al. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 2010;214:519-534.
Levy A, Yen Tran TP, Boucher O, et al. Operculo-insular epilepsy: scalp and intracranial electroencephalographic findings. J Clin Neurophysiol 2017;34:438-447.
Afif A, Chabardes S, Minotti L, et al. Safety and usefulness of insular depth electrodes implanted via an oblique approach in patients with epilepsy. Neurosurgery 2008;62:ONS471-ONS479; discussion 479-480.
Alomar S, Mullin JP, Smithason S, Gonzalez-Martinez J. Indications, technique, and safety profile of insular stereoelectroencephalography electrode implantation in medically intractable epilepsy. J Neurosurg 2018;128:1147-1157.
Trebaul L, Deman P, Tuyisenge V, et al. Probabilistic functional tractography of the human cortex revisited. Neuroimage 2018;181:414-429.
Lacuey N, Zonjy B, Kahriman ES, et al. Homotopic reciprocal functional connectivity between anterior human insulae. Brain Struct Funct 2016;221:2695-2701.
Perucca P, Dubeau F, Gotman J. Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain 2014;137:183-196.
Bartolomei F, Chauvel P, Wendling F. Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 2008;131:1818-1830.
Montavont A, Mauguiere F, Mazzola L, et al. On the origin of painful somatosensory seizures. Neurology 2015;84:594-601.
Peltola ME, Trébuchon A, Lagarde S, et al. Anatomoelectroclinical features of SEEG-confirmed pure insular-onset epilepsy. Epilepsy Behav 2020;105:106964.
Freri E, Matricardi S, Gozzo F, et al. Perisylvian, including insular, childhood epilepsy: presurgical workup and surgical outcome. Epilepsia 2017;58:1360-1369.
Bartolomei F, Lagarde S, Scavarda D, et al. The role of the dorsal anterior insula in ecstatic sensation revealed by direct electrical brain stimulation. Brain Stimul 2019;12:1121-1126.
Mazzola L, Mauguière F, Isnard J. Electrical stimulations of the human insula: their contribution to the ictal semiology of insular seizures. J Clin Neurophysiol 2017;34:307-314.
Chouchou F, Mauguière F, Vallayer O, et al. How the insula speaks to the heart: cardiac responses to insular stimulation in humans. Hum Brain Mapp 2019;40:2611-2622.
Xiao H, Tran TP, Pétrin M, et al. Reflex operculoinsular seizures. Epileptic Disord 2016;18:19-25.
Cloutman LL, Binney RJ, Drakesmith M, et al. The variation of function across the human insula mirrors its patterns of structural connectivity: evidence from in vivo probabilistic tractography. Neuroimage 2012;59:3514-3521.
Almashaikhi T, Rheims S, Jung J, et al. Functional connectivity of insular efferences. Hum Brain Mapp 2014;35:5279-5294.
Ghaziri J, Tucholka A, Girard G, et al. The corticocortical structural connectivity of the human insula. Cereb Cortex 2017;27:1216-1228.
von Lehe M, Wellmer J, Urbach H, et al. Insular lesionectomy for refractory epilepsy: management and outcome. Brain 2009;132:1048-1056.
Boucher O, Rouleau I, Escudier F, et al. Neuropsychological performance before and after partial or complete insulectomy in patients with epilepsy. Epilepsy Behav 2015;43:53-60.
Wang X, Hu W, McGonigal A, et al. Electroclinical features of insulo-opercular epilepsy: an SEEG and PET study. Ann Clin Transl Neurol 2019;6:1165-1177.
Dimova P, de Palma L, Job-Chapron AS, et al. Radiofrequency thermocoagulation of the seizure-onset zone during stereoelectroencephalography. Epilepsia 2017;58:381-392.
Mullatti N, Landre E, Mellerio C, et al. Stereotactic thermocoagulation for insular epilepsy: lessons from successes and failures. Epilepsia 2019;60:1565-1579.
Chen H, Dugan P, Chong DJ, et al. Application of RNS in refractory epilepsy: targeting insula. Epilepsia Open 2017;2:345-349.
Hawasli AH, Bandt SK, Hogan RE, et al. Laser ablation as treatment strategy for medically refractory dominant insular epilepsy: therapeutic and functional considerations. Stereotact Funct Neurosurg 2014;92:397-404.