The impact of epilepsies on brain structure and function

Ana Carolina Coan

doi:10.17724/jicna.2023.289

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June 8, 2023

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August 18, 2023

Published

September 1, 2023

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Abstract

Epilepsies are disorders associated with the dysfunction of the integrity of brain neural networks, leading to changes in physiological interactions and the possible emergence of pathological neural networks. Numerous mechanisms may be associated with alterations in neural networks in epilepsy, including the recurrence of abnormal synchronous neuronal activity during seizures or interictal discharges. The underlying etiology, stage of neurodevelopment in which they occur, and the use of antiseizure medication must also play a significant role in these abnormalities. Additionally, neural network alterations in epilepsy may have a significant relationship with the clinical phenotype, contributing to the unsatisfactory response to pharmacological treatment, as well as the frequent occurrence of neuropsychiatric comorbidities in these disorders. This review presents data on changes in structural and functional brain networks in epilepsies, their relation to specific phenotypes, and their potential impact on the neurodevelopment of children and adolescents.

Keywords

neural network neurodevelopment comorbidities

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Coan, A. C. (2023). The impact of epilepsies on brain structure and function. Journal of the International Child Neurology Association, 1(1). https://doi.org/10.17724/jicna.2023.289

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Funding data

Fundação de Amparo à Pesquisa do Estado de São Paulo
Grant numbers 2022/10175-1

References

Spencer SS. Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia. 2002;43:219-27. URL: https://pubmed.ncbi.nlm.nih.gov/11952791/
van Diessen E, Zweiphenning WJEM, Jansen FE, Stam CJ, Braun KPJ, Otte WM. Brain Network Organization in Focal Epilepsy: A Systematic Review and Meta-Analysis. PLoS One. 2014;9:e114606. URL: https://pubmed.ncbi.nlm.nih.gov/25436868/
Cendes F, Andermann F, Gloor P, et al. Atrophy of mesial structures in patients with temporal lobe epilepsy: cause or consequence of repeated seizures? Ann Neurol. 1993;34:795-801. URL: https://pubmed.ncbi.nlm.nih.gov/8250525/
Liu RS, Lemieux L, Bell GS, et al. Cerebral damage in epilepsy: a population-based longitudinal quantitative MRI study. Epilepsia. 2005;46:1482-94. URL: https://pubmed.ncbi.nlm.nih.gov/16190935/
Pittau F, Grova C, Moeller F, Gotman J. Patterns of altered functional connectivity in mesial temporal lobe epilepsy. 2012;53:1013–23. URL: https://pubmed.ncbi.nlm.nih.gov/22696190/
Coan AC, Campos BM, Beltramini GC, Yasuda CL, Covolan RJM, Cendes F. Distinct functional and structural MRI abnormalities in mesial temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia. 2014;55:1187–96. URL: https://pubmed.ncbi.nlm.nih.gov/24849061/
Whelan CD, Altmann A, Botía JA, et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018;141:391–408. URL: https://pubmed.ncbi.nlm.nih.gov/29272333/
Hatton SN, Huynh KH, Bonilha L, et al. White matter abnormalities across different epilepsy syndromes in adults: an ENIGMA-Epilepsy study. Brain 2020;143: 2454-73. URL: https://pubmed.ncbi.nlm.nih.gov/32766768/
de Campos BM, Coan AC, Lin Yasuda C, Casseb RF, Cendes F. Large‐scale brain networks are distinctly affected in right and left mesial temporal lobe epilepsy. Hum brain mapping. 2016;37(9):3137-3152. URL: https://pubmed.ncbi.nlm.nih.gov/27255148/
Elger CE, Helmstaedter C, Kurthen M. Chronic epilepsy and cognition. Lancet Neurol. 2004;3:663-72. URL: https://pubmed.ncbi.nlm.nih.gov/15488458/
Gowers WR. Epilepsy and Other Chronic Convulsive Diseases. London: Churchill Livingston; 1881.
Coan AC, Appenzeller S, Bonilha L, Li LM, Cendes F. Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy. Neurology. 2009;73:834-42. URL: https://pubmed.ncbi.nlm.nih.gov/19786690/
Coan AC, Campos BM, Yasuda CL, et al. Frequent seizures are associated with a network of gray matter atrophy in temporal lobe epilepsy with or without hippocampal sclerosis. PLoS One. 2014;9:e85843. URL: https://pubmed.ncbi.nlm.nih.gov/24489835/
Campos BM, Coan AC, Beltramini GC, Liu M, Yasuda CL, Ghizoni E, et al. White matter abnormalities associate with type and localization of focal epileptogenic lesions. Epilepsia. 2015;56(1):125-132. URL: https://pubmed.ncbi.nlm.nih.gov/25470376/
Sabaz M, Cairns DR, Lawson JA, Bleasel AF, Bye AM. The health-related quality of life of children with refractory epilepsy: a comparison of those with and without intellectual disability. Epilepsia. 2001;42:621-8. URL: https://pubmed.ncbi.nlm.nih.gov/11380570/
Ben-Ari Y, Holmes GL. Effects of seizures on developmental processes in the immature brain. Lancet Neurol. 2006;5(12):1055-1063. URL: https://pubmed.ncbi.nlm.nih.gov/17110286/
Hermann B, Jones J, Sheth R, Dow C, Koehn M, Seidenberg M. Children with new-onset epilepsy: neuropsychological status and brain structure. Brain. 2006;129:2609-2619. URL: https://pubmed.ncbi.nlm.nih.gov/16893998/
Weglage J, Demsky A, Pietsch M, Kurlemann G. Neuropsychological, intellectual, and behavioral findings in patients with centrotemporal spikes with and without seizures. Dev Med Child Neurol. 1997;39:646-651. URL: https://pubmed.ncbi.nlm.nih.gov/9350140/
Luders E, Narr KL, Bilder RM, et al. Positive correlations between corpus callosum thickness and intelligence. Neuroimage. 2007;37:1457-1464. URL: https://pubmed.ncbi.nlm.nih.gov/17669555/
Hutchinson E, Pulsipher D, Dabbs K, et al. Children with new-onset epilepsy exhibit diffusion abnormalities in cerebral white matter in the absence of volumetric differences. Epilepsy Res. 2010;88:208-214. URL: https://pubmed.ncbi.nlm.nih.gov/19939769/
Hermann B, Hansen R, Seidenberg M, Magnotta V, O'Leary D. Neurodevelopmental vulnerability of the corpus callosum to childhood onset localization-related epilepsy. Neuroimage. 2003;18:284-292. URL: https://pubmed.ncbi.nlm.nih.gov/12595178/
Perani S, Tierney TM, Centeno M, et al. Thalamic volume reduction in drug-naive patients with new-onset genetic generalized epilepsy. Epilepsia. 2018;59:226-234. URL: https://pubmed.ncbi.nlm.nih.gov/29316390/
Tosun D, Dabbs K, Caplan R, Siddarth P, Toga A, Seidenberg M, Hermann B. Deformation-based morphometry of prospective neurodevelopmental changes in new onset paediatric epilepsy. Brain. 2011;134(4):1003-1014. URL: https://pubmed.ncbi.nlm.nih.gov/21478195/
Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci. 2010;14:277-290. URL: https://pubmed.ncbi.nlm.nih.gov/20430461/
Luo C, Li Q, Lai Y, et al. Altered functional connectivity in default mode network in absence epilepsy: a resting-state fMRI study. Hum Brain Mapp. 2011;32:438-449. URL: https://pubmed.ncbi.nlm.nih.gov/20336649/
Widjaja E, Zamyadi M, Raybaud C, Snead OC, Smith ML. Impaired default mode network on resting-state fMRI in children with medically refractory epilepsy. AJNR Am J Neuroradiol. 2013;34:552-557. URL: https://pubmed.ncbi.nlm.nih.gov/22899771/
Oyegbile TO, VanMeter JW, Motamedi GK, et al. Default mode network deactivation in pediatric temporal lobe epilepsy: Relationship to a working memory task and executive function tests. Epilepsy Behav. 2019;94:124-130. URL: https://pubmed.ncbi.nlm.nih.gov/30947003/
Zhang Z, Lu G, Zhong Y, et al. Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res. 2010;1323:152-160. URL: https://pubmed.ncbi.nlm.nih.gov/20188771/
Padmanabhan A, Lynch CJ, Schaer M, Menon V. The default mode network in autism. Biol Psychiatry Cogn Neurosci Neuroimaging. 2017;2(6):476-486. URL: https://pubmed.ncbi.nlm.nih.gov/29529410/
Guimarães CA, Bonilha L, Franzon RC, et al. Distribution of regional gray matter abnormalities in a pediatric population with temporal lobe epilepsy and correlation with neuropsychological performance. Epilepsy Behav. 2007;11:558-566. URL: https://pubmed.ncbi.nlm.nih.gov/17913375/
Overvliet GM, Besseling RM, Jansen JF, et al. Early onset of cortical thinning in children with rolandic epilepsy. Neuroimage Clin. 2013;2:434-439. URL: https://pubmed.ncbi.nlm.nih.gov/24179815/
Luo C, Zhang Y, Cao W, et al. Altered structural and functional feature of striato-cortical circuit in benign epilepsy with centrotemporal spikes. Int J Neural Syst. 2015;25(1):1550027. URL: https://pubmed.ncbi.nlm.nih.gov/25519369/
Northcott E, Connolly AM, Berroya A, et al. The neuropsychological and language profile of children with benign rolandic epilepsy. Epilepsia. 2005;46:924-930. URL: https://pubmed.ncbi.nlm.nih.gov/16060934/
Xiao F, An D, Lei D, et al. Real-time effects of centrotemporal spikes on cognition in rolandic epilepsy: an EEG-fMRI study. Neurology. 2016;86:544-551. URL: https://pubmed.ncbi.nlm.nih.gov/26718591/
Gotman J, Grova C, Bagshaw A, Kobayashi E, Aghakhani Y, Dubeau F. Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. Proc Natl Acad Sci U S A. 2005;102(42):15236-15240. URL: https://pubmed.ncbi.nlm.nih.gov/16217040/
Moeller F, LeVan P, Muhle H, et al. Absence seizures: individual patterns revealed by EEG-fMRI. Epilepsia. 2010;51(10):2000-2010. URL: https://pubmed.ncbi.nlm.nih.gov/20550534/
Moeller F, Siebner HR, Wolff S, et al. Simultaneous EEG-fMRI in drug-naive children with newly diagnosed absence epilepsy. Epilepsia. 2008;49(9):1510-1519. URL: https://pubmed.ncbi.nlm.nih.gov/18557783/
Sidhu MK, Stretton J, Winston GP, et al. Epilepsy and volumetric MRI. Neurology. 2018;91(3):e218-e226. URL: https://pubmed.ncbi.nlm.nih.gov/29970494/
Zuberi SM, Wirrell EC, Yozawitz E, et al. ILAE classification and definition of epilepsy syndromes with onset in neonates and infants: Position statement by the ILAE Task Force on Nosology and Definitions. Epilepsia. 2022;63(6):1349-1397. [https://pubmed.ncbi.nlm.nih.gov/35460545/]
Warren AE, Abbott DF, Vaughan DN, Jackson GD, Archer JS. Abnormal cognitive network interactions in Lennox-Gastaut syndrome: A potential mechanism of epileptic encephalopathy. Epilepsia. 2016;57:812-822. [https://pubmed.ncbi.nlm.nih.gov/26972692/]
Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: Position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58(4):512-521. [https://pubmed.ncbi.nlm.nih.gov/28276062/]
Nicita F, De Liso P, Danti FR, et al. The genetics of monogenic idiopathic epilepsies and epileptic encephalopathies. Seizure. 2012;21(1):3-11. [https://pubmed.ncbi.nlm.nih.gov/22051503/]
Striano P, Zara F. Genetic epilepsies. Eur J Paediatr Neurol. 2011;15(1):88-89. [https://pubmed.ncbi.nlm.nih.gov/20728309/]
Lado FA, Rubboli G, Capovilla G, Avanzini G, Moshé SL. Pathophysiology of Epileptic Encephalopathies. Epilepsia. 2013;54 Suppl 8:6-13. [https://pubmed.ncbi.nlm.nih.gov/24341887/]
Vaessen MJ, Braakman HMH, Heerink JS, et al. Abnormal modular organization of functional networks in cognitively impaired children with frontal lobe epilepsy. Cereb Cortex. 2013;23(9):1997-2006. [https://pubmed.ncbi.nlm.nih.gov/22919083/]
Siniatchkin M, Groening K, Moehring J, et al. Neuronal networks in children with continuous spikes and waves during slow sleep. Brain. 2010;133(Pt 9):2798-2813. [https://pubmed.ncbi.nlm.nih.gov/20701778/]
Archer JS, Warren AE, Stagnitti MR, et al. Lennox-Gastaut syndrome and phenotype: Secondary network epilepsies. Epilepsia. 2014;55(8):1245-1254. [https://pubmed.ncbi.nlm.nih.gov/24930802/]
Archer JS, Warren AE, Jackson GD, Abbott DF. Conceptualizing Lennox-Gastaut syndrome as a secondary network epilepsy. Front Neurol. 2014;5:225. [https://pubmed.ncbi.nlm.nih.gov/25140149/]
Ibrahim GM, Cassel D, Morgan BR, et al. Resilience of developing brain networks to interictal epileptiform discharges is associated with cognitive outcome. Brain. 2014;137(Pt 9):2690-2702. [https://pubmed.ncbi.nlm.nih.gov/25057128/]
Siniatchkin M, Coropceanu D, Moeller F, Boor R, Stephani U. EEG-fMRI reveals activation of brainstem and thalamus in patients with Lennox-Gastaut syndrome. Epilepsia. 2011;52(4):766-774. [https://pubmed.ncbi.nlm.nih.gov/21371059/]
Pillay N, Archer JS, Badawy RA, Flanagan DF, Berkovic SF, Jackson G. Networks underlying paroxysmal fast activity and slow spike and wave in Lennox-Gastaut syndrome. Neurology. 2013;81(7):665-673. [https://pubmed.ncbi.nlm.nih.gov/23940099/]
Siniatchkin M, Van Baalen A, Jacobs J, et al. Different neuronal networks are associated with spikes and slow activity in hypsarrhythmia. Epilepsia. 2007;48(12):2312-2321. [https://pubmed.ncbi.nlm.nih.gov/17919311/]
Coan AC, Cavalcante CM, Burgess RC. Utility of functional MRI and magnetoencephalography in the diagnosis of infantile spasms and hypsarrhythmia. J Clin Neurophysiol. 2022;39(7):544-551. [https://pubmed.ncbi.nlm.nih.gov/34164734/]
Siniatchkin M, Van Bogaert P. Pathophysiology of encephalopathy related to continuous spike and waves during sleep: the contribution of neuroimaging. Epileptic Disord. 2019;21(S2):S48-S53. [https://pubmed.ncbi.nlm.nih.gov/31625533/]

References

Spencer SS. Neural networks in human epilepsy: evidence of and implications for treatment. Epilepsia. 2002;43:219-27. URL: https://pubmed.ncbi.nlm.nih.gov/11952791/

van Diessen E, Zweiphenning WJEM, Jansen FE, Stam CJ, Braun KPJ, Otte WM. Brain Network Organization in Focal Epilepsy: A Systematic Review and Meta-Analysis. PLoS One. 2014;9:e114606. URL: https://pubmed.ncbi.nlm.nih.gov/25436868/

Cendes F, Andermann F, Gloor P, et al. Atrophy of mesial structures in patients with temporal lobe epilepsy: cause or consequence of repeated seizures? Ann Neurol. 1993;34:795-801. URL: https://pubmed.ncbi.nlm.nih.gov/8250525/

Liu RS, Lemieux L, Bell GS, et al. Cerebral damage in epilepsy: a population-based longitudinal quantitative MRI study. Epilepsia. 2005;46:1482-94. URL: https://pubmed.ncbi.nlm.nih.gov/16190935/

Pittau F, Grova C, Moeller F, Gotman J. Patterns of altered functional connectivity in mesial temporal lobe epilepsy. 2012;53:1013–23. URL: https://pubmed.ncbi.nlm.nih.gov/22696190/

Coan AC, Campos BM, Beltramini GC, Yasuda CL, Covolan RJM, Cendes F. Distinct functional and structural MRI abnormalities in mesial temporal lobe epilepsy with and without hippocampal sclerosis. Epilepsia. 2014;55:1187–96. URL: https://pubmed.ncbi.nlm.nih.gov/24849061/

Whelan CD, Altmann A, Botía JA, et al. Structural brain abnormalities in the common epilepsies assessed in a worldwide ENIGMA study. Brain. 2018;141:391–408. URL: https://pubmed.ncbi.nlm.nih.gov/29272333/

Hatton SN, Huynh KH, Bonilha L, et al. White matter abnormalities across different epilepsy syndromes in adults: an ENIGMA-Epilepsy study. Brain 2020;143: 2454-73. URL: https://pubmed.ncbi.nlm.nih.gov/32766768/

de Campos BM, Coan AC, Lin Yasuda C, Casseb RF, Cendes F. Large‐scale brain networks are distinctly affected in right and left mesial temporal lobe epilepsy. Hum brain mapping. 2016;37(9):3137-3152. URL: https://pubmed.ncbi.nlm.nih.gov/27255148/

Elger CE, Helmstaedter C, Kurthen M. Chronic epilepsy and cognition. Lancet Neurol. 2004;3:663-72. URL: https://pubmed.ncbi.nlm.nih.gov/15488458/

Gowers WR. Epilepsy and Other Chronic Convulsive Diseases. London: Churchill Livingston; 1881.

Coan AC, Appenzeller S, Bonilha L, Li LM, Cendes F. Seizure frequency and lateralization affect progression of atrophy in temporal lobe epilepsy. Neurology. 2009;73:834-42. URL: https://pubmed.ncbi.nlm.nih.gov/19786690/

Coan AC, Campos BM, Yasuda CL, et al. Frequent seizures are associated with a network of gray matter atrophy in temporal lobe epilepsy with or without hippocampal sclerosis. PLoS One. 2014;9:e85843. URL: https://pubmed.ncbi.nlm.nih.gov/24489835/

Campos BM, Coan AC, Beltramini GC, Liu M, Yasuda CL, Ghizoni E, et al. White matter abnormalities associate with type and localization of focal epileptogenic lesions. Epilepsia. 2015;56(1):125-132. URL: https://pubmed.ncbi.nlm.nih.gov/25470376/

Sabaz M, Cairns DR, Lawson JA, Bleasel AF, Bye AM. The health-related quality of life of children with refractory epilepsy: a comparison of those with and without intellectual disability. Epilepsia. 2001;42:621-8. URL: https://pubmed.ncbi.nlm.nih.gov/11380570/

Ben-Ari Y, Holmes GL. Effects of seizures on developmental processes in the immature brain. Lancet Neurol. 2006;5(12):1055-1063. URL: https://pubmed.ncbi.nlm.nih.gov/17110286/

Hermann B, Jones J, Sheth R, Dow C, Koehn M, Seidenberg M. Children with new-onset epilepsy: neuropsychological status and brain structure. Brain. 2006;129:2609-2619. URL: https://pubmed.ncbi.nlm.nih.gov/16893998/

Weglage J, Demsky A, Pietsch M, Kurlemann G. Neuropsychological, intellectual, and behavioral findings in patients with centrotemporal spikes with and without seizures. Dev Med Child Neurol. 1997;39:646-651. URL: https://pubmed.ncbi.nlm.nih.gov/9350140/

Luders E, Narr KL, Bilder RM, et al. Positive correlations between corpus callosum thickness and intelligence. Neuroimage. 2007;37:1457-1464. URL: https://pubmed.ncbi.nlm.nih.gov/17669555/

Hutchinson E, Pulsipher D, Dabbs K, et al. Children with new-onset epilepsy exhibit diffusion abnormalities in cerebral white matter in the absence of volumetric differences. Epilepsy Res. 2010;88:208-214. URL: https://pubmed.ncbi.nlm.nih.gov/19939769/

Hermann B, Hansen R, Seidenberg M, Magnotta V, O'Leary D. Neurodevelopmental vulnerability of the corpus callosum to childhood onset localization-related epilepsy. Neuroimage. 2003;18:284-292. URL: https://pubmed.ncbi.nlm.nih.gov/12595178/

Perani S, Tierney TM, Centeno M, et al. Thalamic volume reduction in drug-naive patients with new-onset genetic generalized epilepsy. Epilepsia. 2018;59:226-234. URL: https://pubmed.ncbi.nlm.nih.gov/29316390/

Tosun D, Dabbs K, Caplan R, Siddarth P, Toga A, Seidenberg M, Hermann B. Deformation-based morphometry of prospective neurodevelopmental changes in new onset paediatric epilepsy. Brain. 2011;134(4):1003-1014. URL: https://pubmed.ncbi.nlm.nih.gov/21478195/

Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci. 2010;14:277-290. URL: https://pubmed.ncbi.nlm.nih.gov/20430461/

Luo C, Li Q, Lai Y, et al. Altered functional connectivity in default mode network in absence epilepsy: a resting-state fMRI study. Hum Brain Mapp. 2011;32:438-449. URL: https://pubmed.ncbi.nlm.nih.gov/20336649/

Widjaja E, Zamyadi M, Raybaud C, Snead OC, Smith ML. Impaired default mode network on resting-state fMRI in children with medically refractory epilepsy. AJNR Am J Neuroradiol. 2013;34:552-557. URL: https://pubmed.ncbi.nlm.nih.gov/22899771/

Oyegbile TO, VanMeter JW, Motamedi GK, et al. Default mode network deactivation in pediatric temporal lobe epilepsy: Relationship to a working memory task and executive function tests. Epilepsy Behav. 2019;94:124-130. URL: https://pubmed.ncbi.nlm.nih.gov/30947003/

Zhang Z, Lu G, Zhong Y, et al. Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res. 2010;1323:152-160. URL: https://pubmed.ncbi.nlm.nih.gov/20188771/

Padmanabhan A, Lynch CJ, Schaer M, Menon V. The default mode network in autism. Biol Psychiatry Cogn Neurosci Neuroimaging. 2017;2(6):476-486. URL: https://pubmed.ncbi.nlm.nih.gov/29529410/

Guimarães CA, Bonilha L, Franzon RC, et al. Distribution of regional gray matter abnormalities in a pediatric population with temporal lobe epilepsy and correlation with neuropsychological performance. Epilepsy Behav. 2007;11:558-566. URL: https://pubmed.ncbi.nlm.nih.gov/17913375/

Overvliet GM, Besseling RM, Jansen JF, et al. Early onset of cortical thinning in children with rolandic epilepsy. Neuroimage Clin. 2013;2:434-439. URL: https://pubmed.ncbi.nlm.nih.gov/24179815/

Luo C, Zhang Y, Cao W, et al. Altered structural and functional feature of striato-cortical circuit in benign epilepsy with centrotemporal spikes. Int J Neural Syst. 2015;25(1):1550027. URL: https://pubmed.ncbi.nlm.nih.gov/25519369/

Northcott E, Connolly AM, Berroya A, et al. The neuropsychological and language profile of children with benign rolandic epilepsy. Epilepsia. 2005;46:924-930. URL: https://pubmed.ncbi.nlm.nih.gov/16060934/

Xiao F, An D, Lei D, et al. Real-time effects of centrotemporal spikes on cognition in rolandic epilepsy: an EEG-fMRI study. Neurology. 2016;86:544-551. URL: https://pubmed.ncbi.nlm.nih.gov/26718591/

Gotman J, Grova C, Bagshaw A, Kobayashi E, Aghakhani Y, Dubeau F. Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. Proc Natl Acad Sci U S A. 2005;102(42):15236-15240. URL: https://pubmed.ncbi.nlm.nih.gov/16217040/

Moeller F, LeVan P, Muhle H, et al. Absence seizures: individual patterns revealed by EEG-fMRI. Epilepsia. 2010;51(10):2000-2010. URL: https://pubmed.ncbi.nlm.nih.gov/20550534/

Moeller F, Siebner HR, Wolff S, et al. Simultaneous EEG-fMRI in drug-naive children with newly diagnosed absence epilepsy. Epilepsia. 2008;49(9):1510-1519. URL: https://pubmed.ncbi.nlm.nih.gov/18557783/

Sidhu MK, Stretton J, Winston GP, et al. Epilepsy and volumetric MRI. Neurology. 2018;91(3):e218-e226. URL: https://pubmed.ncbi.nlm.nih.gov/29970494/

Zuberi SM, Wirrell EC, Yozawitz E, et al. ILAE classification and definition of epilepsy syndromes with onset in neonates and infants: Position statement by the ILAE Task Force on Nosology and Definitions. Epilepsia. 2022;63(6):1349-1397. [https://pubmed.ncbi.nlm.nih.gov/35460545/]

Warren AE, Abbott DF, Vaughan DN, Jackson GD, Archer JS. Abnormal cognitive network interactions in Lennox-Gastaut syndrome: A potential mechanism of epileptic encephalopathy. Epilepsia. 2016;57:812-822. [https://pubmed.ncbi.nlm.nih.gov/26972692/]

Scheffer IE, Berkovic S, Capovilla G, et al. ILAE classification of the epilepsies: Position paper of the ILAE Commission for Classification and Terminology. Epilepsia. 2017;58(4):512-521. [https://pubmed.ncbi.nlm.nih.gov/28276062/]

Nicita F, De Liso P, Danti FR, et al. The genetics of monogenic idiopathic epilepsies and epileptic encephalopathies. Seizure. 2012;21(1):3-11. [https://pubmed.ncbi.nlm.nih.gov/22051503/]

Striano P, Zara F. Genetic epilepsies. Eur J Paediatr Neurol. 2011;15(1):88-89. [https://pubmed.ncbi.nlm.nih.gov/20728309/]

Lado FA, Rubboli G, Capovilla G, Avanzini G, Moshé SL. Pathophysiology of Epileptic Encephalopathies. Epilepsia. 2013;54 Suppl 8:6-13. [https://pubmed.ncbi.nlm.nih.gov/24341887/]

Vaessen MJ, Braakman HMH, Heerink JS, et al. Abnormal modular organization of functional networks in cognitively impaired children with frontal lobe epilepsy. Cereb Cortex. 2013;23(9):1997-2006. [https://pubmed.ncbi.nlm.nih.gov/22919083/]

Siniatchkin M, Groening K, Moehring J, et al. Neuronal networks in children with continuous spikes and waves during slow sleep. Brain. 2010;133(Pt 9):2798-2813. [https://pubmed.ncbi.nlm.nih.gov/20701778/]

Archer JS, Warren AE, Stagnitti MR, et al. Lennox-Gastaut syndrome and phenotype: Secondary network epilepsies. Epilepsia. 2014;55(8):1245-1254. [https://pubmed.ncbi.nlm.nih.gov/24930802/]

Archer JS, Warren AE, Jackson GD, Abbott DF. Conceptualizing Lennox-Gastaut syndrome as a secondary network epilepsy. Front Neurol. 2014;5:225. [https://pubmed.ncbi.nlm.nih.gov/25140149/]

Ibrahim GM, Cassel D, Morgan BR, et al. Resilience of developing brain networks to interictal epileptiform discharges is associated with cognitive outcome. Brain. 2014;137(Pt 9):2690-2702. [https://pubmed.ncbi.nlm.nih.gov/25057128/]

Siniatchkin M, Coropceanu D, Moeller F, Boor R, Stephani U. EEG-fMRI reveals activation of brainstem and thalamus in patients with Lennox-Gastaut syndrome. Epilepsia. 2011;52(4):766-774. [https://pubmed.ncbi.nlm.nih.gov/21371059/]

Pillay N, Archer JS, Badawy RA, Flanagan DF, Berkovic SF, Jackson G. Networks underlying paroxysmal fast activity and slow spike and wave in Lennox-Gastaut syndrome. Neurology. 2013;81(7):665-673. [https://pubmed.ncbi.nlm.nih.gov/23940099/]

Siniatchkin M, Van Baalen A, Jacobs J, et al. Different neuronal networks are associated with spikes and slow activity in hypsarrhythmia. Epilepsia. 2007;48(12):2312-2321. [https://pubmed.ncbi.nlm.nih.gov/17919311/]

Coan AC, Cavalcante CM, Burgess RC. Utility of functional MRI and magnetoencephalography in the diagnosis of infantile spasms and hypsarrhythmia. J Clin Neurophysiol. 2022;39(7):544-551. [https://pubmed.ncbi.nlm.nih.gov/34164734/]

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