Sleep is a Major Participant of Epileptogenesis in Physiological Brain Networks

Main Article Content

Péter Halász Anna Szűcs

Abstract

We aimed to provide a comprehensive review of the system epilepsy concept and adapt its principles to major epilepsy syndromes. We present our views on epileptogenesis: NREM sleep and especially sleep homeostatic plasticity are essential contributors of the epileptic transformation, upgrading and derailing normal brain networks. We follow the common process and specific features epileptic transformation in major epilepsies.

Keywords: sleep homeostatic power, plasticity, epileptogenesis, interictal epileptiform discharges, system-epilepsy

Article Details

How to Cite
HALÁSZ, Péter; SZŰCS, Anna. Sleep is a Major Participant of Epileptogenesis in Physiological Brain Networks. Medical Research Archives, [S.l.], v. 12, n. 11, nov. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5953>. Date accessed: 12 dec. 2024. doi: https://doi.org/10.18103/mra.v12i11.5953.
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Research Articles

References

1. Pitkänen A, Engel J Jr. Past and present definitions of epileptogenesis and its biomarkers. Neurotherapeutics. 2014;11(2):231-41. Doi:10.1007/s13311-014-0257-2.
2. Klein P, Dingledine R, Aronica E, et al. Commonalities in epileptogenic processes from different acute brain insults: Do they translate? Epilepsia.2018;59(1):37-66. Doi:10.1111/epi.13965.
3. Steriade M. Neuronal substrates of sleep and epilepsy. Cambridge: University Press. 2003.
4. Goddard GV, McIntyre D, Leech C. A permanent change in brain function resulting from daily electrical stimulation. Exp. Neurol 1969; 25:295–330.
5. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973;232(2):331-56.
6. Wada JA, Sato M. Generalized convulsive seizure state induced by daily stimulation of the amygdala in split-brain cats. Paper presented at the 27th annual meeting of the American Electroencephalographic Society. 1973. Boston.
7. Morrell F. Goddard’s kindling phenomenon: A new model of the “mirror focus”. In: H. C. Sabel Ji (Ed.) Chemical modulation of brain New York: Raven 1973
8. Morrell F, deToledo-Morrell L. From mirror focus to secondary epileptogenesis in man:an historical review. Adv Neurol 1999;81:11-23.
9. Tononi G, Cirelli C. Sleep and synaptic homeostasis: a hypothesis. Brain Research Bulletin 2003;62(2):143-50.
10. Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Medicine Reviews 2006;10(1):49–62.
11. Tononi G, Cirelli C. Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 2014; 81(1):12-34.
12. Gibbs: Gibbs FA, Gibbs EL. Atlas of electroenecephalography 1,2 1950.
13. Nobili L, Frauscher B, Eriksson S, et al. Sleep and epilepsy: A snapshot of knowledge and future research lines. J Sleep Res. 2022;31(4):e13622.
14. Beenhakker MP, Huguenard JR. Neurons that fire together also conspire together: is normal sleep circuitry hijacked to generate epilepsy? Neuron 2009;62:612–32.
15. Halász P. Are absence epilepsy and nocturnal frontal lobe epilepsy system epilepsies of the sleep/wake system? Behav Neurol 2015; 231676
16. Avanzini G, Manganotti P, Meletti S, et al. The system epilepsies: a pathophysiological hypothesis. Epilepsia. 2012; 53: 71-8
17. Wolf P, Yacubian EM, Avanzini G, et al. Juvenile myoclonic epilepsy: A system disorder of the brain. Epilepsy Res 2015;114:2-12.
18. Striano P, Striano S. Reading epilepsy and its variants: a model for system epilepsy. Epilepsy Behav. 2011;20(3):591. Doi:10.1016/j.yebeh.2011.01.021
19. Halász P, Kelemen A, Clemens B, et al. The perisylvian epileptic network. A unifying concept. Ideggyogy Sz. 2005; 5920;58(1-2):21-31
20. Szűcs A, Rosdy B, Kelemen A, Horváth A, Halász P. Reflex seizure triggering: Learning about seizure producing systems. Seizure. 2019;69:25-30. Doi:10.1016/j.seizure.2019.03.019.
21. Scoville WB, Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 1957;20(1):11–21. Doi:10.1136/jnnp.20.1.11.
22. Born J. Rasch B. Gais S. Sleep to remember. Neuroscientist 2006;12(5):410-24.
23. Rasch B, Born J. About sleep’s role in memory. Physiol Rev 2013;93(2):681-766. Doi:10.1152/physrev.00032.2012
24. Buzsáki G. Hippocampal Sharp Wave-Ripple: A cognitive Biomarker for Episodic Memory and Planning. Hippocampus. 2015;25–8, 10738
25. Clemens Z, Mölle M, Erőss L, et al. Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur J Neuro Sci. 2011;33:511-20
26. Latchoumane CV, Ngo HV, Born J, Shin, HS. Thalamic spindles promote memory formation during sleep through triple phase-locking of cortical, thalamic, and a hippocampal rhythms. Neuron. 2018;95:424–35.
27. Staresina BP, Niediek J, Borger V, Surges R, Mormann F. How coupled slow oscillations, spindles and ripples coordinate neuronal processing and communication during human sleep. Nat Neurosci. 2023;26(8):1429-37. Doi:10.1038/s41593-023-01381-w.
28. Mölle M, Born J. Slow oscillations orchestrating fast oscillations and memory consolidation. Prog Brain Res. 2011;193:93-110. Doi:10.1016/B978-0-444-53839-0.00007-7.
29. Fogel SM, Smith CT. Learning-dependent changes in sleep spindles and Stage 2 sleep. J Sleep Res. 2006;15:250–5.
30. Gais S, Molle M, Helms K, Born J. Learning-dependent increases in sleep spindle density. J Neurol Sci. 2002;22:6830–4.
31. Schabus M, Gruber G, Parapatics S, et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 2004;27(8):1479-85.Doi:10.1093/sleep/27.7.1479.
32. Jackson JH. On a particular variety of epilepsy (“intellectual aura”), one case with symptoms of organic brain disease. Brain. 1888;11:179–207. Doi:10.1093/brain/11.2.179
33. Penfield W, Jasper HH. Epilepsy and the Functional Anatomy of the Human Brain.1954. Little Brown and Company – Boston.
34. Bancaud J, Talairach J. Sémiologie clinique des crises du lobe temporal (méthodologie et investigations SEEG de 233 malades). In: Crises épileptiques et épilepsies du lobe temporal, tome II. Gentilly: documentation médicale Labaz, 1991. Boston: 1954 Little, Brown
35. Sano K, Malamud N. Clinical significance of sclerosis of the cornu Ammonis: ictal psychic phenomena. Arch. Neurol. Psychiat (Chic.) 1953;70:40–53.
36. Margerison JH, Corsellis JA. Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain. 1966;89(3):499-530. Doi:10.1093/brain/89.3.4991007
37. Babb TL, Kupfer WR, Pretorius JK, Crandall PH, Levesque MF. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience. 1991;42:351-63.
38. Represa A, Pollard H, Moreau J, Ghilini G, Khrestchatisky M, Ben-Ari Y. Mossy fiber sprouting in epileptic rats is associated with a transient increased expression of alpha-tubulin. Neurosci Lett. 1993;156(1-2):149-52. Doi:10.1016/0304-3940(93)90460-3
39. Tauck DL, Nadler JV. Evidence of functional mossy fiber sprouting in hippocampal formation of kainic acid-treated rats. J Neurosci 1985;5:1016-22.
40. Turski WA, Cavalheiro EA, Schwarz M, Czuczwar SJ, Kleinrok Z, Turski L. Limbic seizures produced by pilocarpine in rats: behavioural, electroencephalographic and neuropathological study. Behav Brain Res. 1983;9:315-35.
41. Maglóczky Z, Freund TF. Impaired and repaired inhibitory circuits in the epileptic human hippocampus. Trends Neurosci. 2005;28(6):334-40. Doi:0.1016/j.tins.2005 04.002
42. Clemens Z, Janszky J, Szűcs A, Békésy M, Clemens B, Halász P. Interictal epileptic spiking during sleep and wakefulness in mesial temporal lobe epilepsy: a comparative study of scalp and foramen ovale electrodes. Epilepsia 2003;44:186-92.
43. Shatskikh TN, Raghavendra M, Zhao Q, Cui Z, Holmes GL. Electrical induction of spikes in the hippocampus impairs recognition capacity and spatial memory in rats. Epilepsy Behav. 2006;9:549-56
44. Kleen J, Scott RC, Holmes GL, et al. Hippocampal interictal epileptiform activity disrupts cognition in humans. Neurology. 20131:18–24.
45. Lambert I, Tramoni-Negre E, Lagarde S, et al. Accelerated long-term forgetting in focal epilepsy: Do interictal spikes during sleep matter? Epilepsia. 2021;62(3):563-569. Doi:10.1111/epi.16823
46. Gelinas JN, Khodagholy D, Thesen T, Devinsky O, Buzsáki G. Interictal epileptiform discharges induce hippocampal-cortical coupling in temporal lobe epilepsy. Nat Med. 2016;22: 641-8.
47. Frauscher B, Bernasconi N, Caldairou B, von Ellenrieder N, Bernasconi A, Gotman J. Interictal Hippokampal Spiking Influences the Occurrence of Hippokampal Sleep Spindles. Sleep 2015;38(12):1927-33. Doi:10.5665/sleep.5242.
48. Gloor P. Generalized cortico-reticular epilepsies. Some considerations on the pathophysiology of generalized bilaterally synchronous spike and wave discharge. Epilepsia. 1968;9(3):249-63. Doi:10.1111/j.1528-1157.1968.tb04624.x.
49. Frauscher B, Bartolomei F, Kobayashi K, et al. High-frequency oscillations: The state of clinical research. Epilepsia. 2017;58(8):1316-1329. Doi:10.1111/epi.13829.
50. Gulyás AI, Freund TT. Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation. Curr Opin Neurobiol. 2015;31:26-32. Doi:10.1016/j.conb.2014.07.020.
51. Hermann B, Seidenberg M, Lee EJ, Chan F, Rutecki P. Cognitive phenotypes in temporal lobe epilepsy. J Int Neuropsychol Soc. 2007;13(1):12-20.
52. Hermann B, Conant LL, Cook CJ, et al. Network, clinical and sociodemographic features of cognitive phenotypes in temporal lobe epilepsy. Neuroimage Clin 2020;27:102341. Doi:10.1016/j.nicl.2020
53. Steriade M. (2003). Neuronal substrates of sleep and epilepsy. Cambridge University Press, 322-48
54. Steriade M. Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb Cortex. 1997;7(6):583-604.
55. von Krosigk M, Bal T, McCormick DA. Cellular mechanisms of a synchronized oscillation in the thalamus. Science. 1993;261:361–4.
56. Steriade M, Contreras D. Relations between cortical and thalamic cellular events during transition from sleep patterns to paroxysmal activity. J Neurosci. 1995;15(1 Pt 2):623-42
57. Crunelli V, Lőrincz ML, McCafferty C, et al. Clinical and experimental insight into pathophysiology, comorbidity and therapy of absence seizures, Brain, 143(8),2020, 2341–68.
58. Meeren H, Pijn JP, Van Luijtelaar EL, Coenen AM, Lopes da Silva FH. Cortical focus drives widespread corticothalamic networks during spontaneous absence model of corticoreticular epilepsy. Trans Am Neurol Assoc. 2002;98:203–5.
59. Meeren H, van Luijtelaar G, Lopes da Silva F, Coenen A. Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. Arch Neurol. 2005;62:37.
60. Moeller F, Siebner HR, Wolff S, et al. Simultaneous EEG-fMRI in drug-naive children with newly diagnosed absence epilepsy. Epilepsia. 2008;49(9):1510-9. Doi:10.1111/j.1528-1167.2008.01626.x.
61. Aung T, Tenney JR, Bagić AI. Contributions of Magnetoencephalography to Understanding Mechanisms of Generalized Epilepsies: Blurring the Boundary Between Focal and Generalized Epilepsies? Front Neurol. 2022 ;13:831546. Doi:10.3389/fneur.2022.831546.
62. Bancaud J, Talairach J, Morel P, et al. "Generalized" epileptic seizures elicited by electrical stimulation of the frontal lobe in man. Electroencephalogr Clin Neurophysiol. 1974; 37(3):275-82. Doi:10.1016/0013-4694
63. Jocić-Jakubi B, Jovanović M, Janković DS, et al. Frontal-onset absences in children: associated with worse outcome? A replication study. Seizure. 2009 May;18(4):275-8. Doi:10.1016/j.seizure.2008.10.013.
64. Chaitanya G, Sinha S, Narayanan M, Satishchandra P. Scalp high frequency oscillations (HFOs) in absence epilepsy: An independent component analysis (ICA) based approach. Epilepsy Res. 2015;115:133-40. Doi:10.1016/j.eplepsyres.2015.06.008
65. Manning JP, Richards DA, Leresche N, Crunelli V, Bowery NG. Cortical area-specific block of genetically determined absence seizures by ethosuximid. Neuroscience 2004;123:5–9
66. Aghakhani Y, Bagshaw AP, Bénar CG, Hawco C, Andermann F, Dubeau F, et al. fMRI activation during spike and wave discharges in idiopathic generalized epilepsy. Brain 2004; 127: 1127–44.
67. Nehlig A, Valenti MP, Thiriaux A, Hirsch E, Marescaux C, Namer IJ. Ictal and interictal perfusion variations measured by SISCOM analysis in typical childhood absence seizures. Epileptic Disord. 2004;6(4):247-53.
68. Theodore WH, Gaillard WD. Neuroimaging and the progression of epilepsy. Prog Brain Res. 2002;135:305-13. Doi:10.1016/S0079-6123(02)35028-3.
69. McCafferty C, Gruenbaum BF, Tung R, Li JJ, Zheng X, Salvino P, et al. Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures. Nat Commun. 2023;14(1):117. Doi:10.1038/s41467-022-35535-4.
70. Halász P, Dévényi E. Petit mal absences in night sleep with special reference to transitional sleep and REM periods. Acta Med Acad Sci Hung. 1974;31:31. 65
71. Coenen AML, Drinkenburg W, Peeters B. Absence epilepsy and the level of vigilance in rats of the WAG/Rij strain. Neuroscience Biobehavioral Reviews. 1991;15:259-63.
72. Halász P, Bódizs R. Dynamic Structure of NREM Sleep, London, UK: Springer-Verlag London Ltd. 2013. https://doi.org/10.1007/978-1-4471-4333-8.
73. Halász P, Terzano MG, Parrino L. Spike-wave discharge and the microstructure of sleep-wake continuum in idiopathic generalised epilepsy. Neurophysiol Clin. 2002; 32(1):38-53. Doi:10.1016/s0987-7053(01)00290-8.
74. Bagshaw AP, Cendes F. Sleep onset uncovers thalamic abnormalities in patients with idiopathic generalized epilepsy NeuroImage: Clinical. 2017;16:52-5.
75. Suntsova N, Kumar S, Guzman-Marin R, Alam MN, Szymusiak R, McGinty D. A role for the preoptic sleep-promoting system in absence epilepsy. Neurobiol Dis. 2009;36(1):126-41. Doi:10.1016/j.nbd.2009.07.005.
76. Wirrell EC, Camfield CS, Camfield PR, Gordon KE, Dooley JM. Long-term prognosis of typical childhood absence epilepsy: remission or progression to juvenile myoclonic epilepsy. Neurology. 1996;47(4):912-8. Doi:10.1212/wnl.47.4.912.
77. Trinka E, Baumgartner S, Unterberger I, et al. Long-term prognosis for childhood and juvenile absence epilepsy. J Neurol. 2004;251(10):1235-41. Doi:10.1007/s00415-004-0521-1.
78. Gigli GL, Calia E, Marciani MG, et al. Sleep microstructure and EEG epileptiform activity in patients with juvenile myoclonic epilepsy. Epilepsia. 1992;33(5):799-804. Doi:10.1111/j.1528-1157.1992.tb02184.x.
79. Manganotti P, Bongiovanni LG, Fuggetta G, Zanette G, Fiaschi A. Effects of sleep deprivation on cortical excitability in patients affected by juvenile myoclonic epilepsy: a combined transcranial magnetic stimulation and EEG study. J Neurology, Neurosurgery, Psychiatry 2006;77(1):56-60.
80. Wolf P, Goosses R. Relation of photosensitivity to epileptic syndromes. J Neurol Neurosurg Psychiatry. 1986;49(12):1386-91. Doi:10.1136/jnnp.49.12.13861986
81. Uchida CGP, de Carvalho KC, Guaranha MSB, Guilhoto LMFF, de Araújo Filho GM, Yacubian EMT. Prognosis of Juvenile myoclonic epilepsy with eye-closure sensitivity. Seizure. 2018;62:17-25. Doi:10.1016/j.seizure.2018.09.006.
82. Vollmar C, O'Muircheartaigh J, Symms MR, et al. Altered microstructural connectivity in juvenile myoclonic epilepsy: the missing link. Neurology. 2012;78(20):1555-9. Doi:10.1212/WNL.0b013e3182563b44.
83. Wandschneider B, Thompson PJ, Vollmar C, Koepp MJ. Frontal lobe function and structure in juvenile myoclonic epilepsy: a comprehensive review of neuropsychological and imaging data. Epilepsia. 2012;53(12):2091-8. Doi:
84. Koepp MJ, Woermann F, Savic I, Wandschneider B. Juvenile myoclonic epilepsy-neuroimaging findings. Epilepsy Behav. 2013;28 Suppl 1:S40-4. Doi:10.1016/j.yebeh.2012.06.035.
85. Mahowald MW, Schenck CH. Status dissociatus - A perspective on states of being. Sleep. 1991;14(1):69–79
86. .Lyamin OI, Mukhametov LM, Siegel JM, Nazarenko EA, Polyakova IG, Shpak OV. Uni-hemispheric slow wave sleep and the state of the eyes in a white whale. Behav Brain Res. 2002;129(1-2):125-9. Doi:10.1016/s0166-4328(01)00346-1
87. .Rattenborg NC, van der Meij J, Beckers GJL et al. Local aspects of avian non-REM and REM Sleep. Front Neurosci 2019;13:567. https://doi.org/10.3389/fnins.2019.00567
88. .Mascetti GG. Unihemispheric sleep and asymmetrical sleep: behavioral, neurophysiological, and functional perspectives. Nat Sci Sleep 2016; 8:221–238
89. Lugaresi E, Cirignotta F, Montagna P. Nocturnal paroxysmal dystonia. J Neurol Neurosurg Psychiatry 1986;49(4):375–80. Doi:10.1136/jnnp.49.4.375
90. Provini F, Plazzi G, Tinuper P, Vandi S, Lugaresi E, Montagna P. Nocturnal frontal lobe epilepsy. A clinical and polygraphic overview of 100 consecutive cases. Brain. 1999;122(Pt 6):1017-31. Doi:10.1093/brain/122.6.1017.
91. Nobili L, Francione S, Mai R, Tassi L, Cardinale F. Nocturnal frontal lobe epilepsy: intracerebral recordings of paroxysmal motor attacks with increasing complexity. Sleep 2003;26:883–6
92. Oldani A, Zucconi M, Asselta R, et al. Autosomal dominant nocturnal frontal lobe epilepsy. A video-polysomnographic and genetic appraisal of 40 patients and delineation of the epileptic syndrome. Brain. 1998;121(Pt2):205-23. Doi:10.1093/brain/121.2.205.
93. Tinuper P, Bisulli F J. Cross H, et al. Definition and diagnostic criteria of sleep-related hypermotor epilepsy. Neurology 2016;86(19):1834–42. Doi:10.1212/WNL.0000000000002666
94. Celesia GG, Jasper HH. Acetylcholine released from cerebral cortex in relation to state of activation. Neurology. 1966;16(11):1053-63. Doi:10.1212/wnl.16.11.1053.
95. Muzur A, Pace-Schott EF, Hobson JA. The prefrontal cortex in sleep. Trends in Cognitive Sciences. 2002;6(11):475–81
96. Descarries L, Gisiger V, Steriade M. Diffuse transmission by acetylcholine in the CNS. Progress in Neurobiology. 1997;53:603–25.
97. Scheffer IE, Bhatia KP, Lopes-Cendes I, et al. Autosomal dominant nocturnal frontal lobe epilepsy. A distinctive clinical order. Brain.1995;118( Pt 1):61-73. Doi:10.1093/brain/118.1.61/WNL.0000000000002666.
98. Vallés AS, Barrantes FJ. Nicotinic Acetylcholine Receptor Dysfunction in Addiction and in Some Neurodegenerative and Neuropsychiatric Diseases. Cells. 2023;12(16):2051.https://doi.org/10.3390/
99. Han ZY, Le Novère N, Zoli M, Hill JA Jr., Champtiaux JP. Localization of nAChR subunit mRNAs in the brain of Macaca mulatta. Eur J Neuroscience. 2000;12:3664–74.
100. Picard F, Bruel D, Servent D, et al. Alteration of the in vivo nicotinic receptor density in ADNFLE patients: a PET study. Brain. 2006;129(Pt 8):2047-60. Doi:10.1093/brain/awl156
101. Broughton RJ. Sleep disorders: disorders of arousal? Enuresis, somnambulism, and nightmares occur in con-fusional states of arousal, not in “dreaming sleep”. Science. 1968; 159:1070–8. 10.1126/science.159.3819.1070
102. Derry CP, Harvey AS, Walker MC, Duncan JS, Berkovic SF. NREM arousal parasomnias and their distinction from nocturnal frontal lobe epilepsy: a video EEG analysis. Sleep. 2009;32:1637-44.
103. Tassinari CA , Rubboli G, Gardella E, Cantalupo G, Calandra- Buonaura, Vedovello G. Common Semiology in Fronto-Limbic Seizures and in Parasomnias. A Neuroethologic Approach. Neurol Sci. 2005;26 Suppl 3:s225-32. Doi:10.1007/s10072-005-0492-8.
104. Halász P, Simor P, Szűcs A. Fearful arousals in sleep terrors and sleep-related hypermotor epileptic seizures may involve the salience network and the acute stress response of Cannon and Selye. Epilepsy Behav Rep. 2024;25:100650. Doi:10.1016/j.ebr.2024.100650.
105. Mahowald MW, Schenck CH. Status dissociatus - A perspective on states of being. Sleep. 1991;14(1):69–79.
106. Bassetti C, Vella S, Donati F, Wielepp P, Weder B. SPECT during sleepwalking. Lancet. 2000;356(9228):484-5. Doi:10.1016/S0140-6736(00)02561-7.
107. Terzaghi M, Sartori I, Tassi L, et al. Evidence of dissociated arousal states during NREM parasomnia from an intracerebral neurophysiological study. Sleep. 2009;32(3):409-12. Doi:10.1093/sleep/32.3.409.
108. Januszko P, Niemcewicz S, Gajda T, et al. Sleepwalking episodes are preceded by arousal-related activation in the cingulate motor area: EEG current density imaging. Clin Neurophysiol. 2016;127(1):530-536. Doi:10.1016/j.clinph.2015.01.014.
109. Provini F, Plazzi G, Tinuper P, Vandi S, Lugaresi E, Montagna P. Nocturnal frontal lobe epilepsy. A clinical and polygraphic overview of 100 consecutive cases. Brain. 1999;122(Pt 6):1017-31. Doi:10.1093/brain/122.6.1017.
110. Bisulli F, Vignatelli L, Naldi I, et al. Increased frequency of arousal parasomnias in families with nocturnal frontal lobe epilepsy: a common mechanism? Epilepsia. 2010;519:1852–60.
111. Licchetta L, Pippucci T, Baldassari S, et al. Collaborative Group of Italian League Against Epilepsy (LICE) Genetic Study Group on SHE. Sleep-related hypermotor epilepsy (SHE): Contribution of known genes in 103 patients. Seizure. 2020;74:60-64. Doi:10.1016/j.seizure.2019.11.009.
112. Yang Y, Tuo J, Zhang J, Xu Z, Luo Z. Pathogenic genes implicated in sleep-related hypermotor epi-lepsy: a research progress update. Front Neurol. 2024;15:1416648. Doi:10.3389/fneur.2024.1416648.
113. Mutti C, Bernabè G, Barozzi N, et al. Commonalities and Differences in NREM Parasomnias and Sleep-Related Epilepsy: Is There A Continuum Between the Two Conditions? Front Neurol. 2020;11:600026. Doi:10.3389/fneur.2020.600026
114. Halász P, Kelemen A, Szücs A. Physiopathogenetic interrelationship between nocturnal frontal lobe epilepsy and NREM arousal parasomnias. Epilepsy Res Treat. 2012;2012:312693. https://doi.org/10.1016/j.sleep. 2015.05.006
115. Specchio N, Wirrell EC, Scheffer IE, et al. International League Against Epilepsy classification and definition of epilepsy syndromes with onset in childhood: Position paper by the ILAE Task Force on Nosology and Definitions. Epilepsia. 2022;63(6):1398-42. Doi:10.1111/epi.17241.
116. Fortini S, Espeche A, Galicchio S, et al. More than one self-limited epilepsy of childhood in the same patient: A multicenter study. Epilepsy Res. 2021;177:106768. Doi:10.1016/j.eplepsyres.2021.106768
117. Koutroumanidis M, Panayiotopoulos CP. Benign childhood seizure susceptibility syndromes. In: Rugg-Gunn RJ, Smalls JE, editors. From channels to commissioning – a practical guide to epilepsy. London: International League Against Epilepsy (UK Chapter and Epilepsy Society; 2015. Pp:89-113). (2022) 63:1398– 442. https://doi.org/10.1111/epi.1724110.1002/ana.20319
118. Catani M, Jones DK. ffytche DH. Perisylvian language networks of the human brain. Ann Neurol. 2005;57:8-16. https://doi.org/10.1002/ana.20319.
119. Schomers MR, Garagnani M, Pulvermüller F. Neurocomputational consequences of evolutionary connectivity changes in perisylvian language cortex. J Neuroscience. 2017;37(11):3045–55. https://doi.org/10.1523/JNEUROSCI.2693-16.2017.
120. Bouma PA, Bovenkerk AC, Westendorp RG, Brouwer OF. The course of benign partial epilepsy of childhood with centrotemporal spikes: a meta-analysis. Neurology. 1997;48(2):430-7. Doi:10.1212/ wnl.48.2.430.
121. Clemens B, Majoros E. Sleep studies in benign epilepsy of childhood with Rolandic spikes. II. Analysis of discharge frequency and its relation to sleep dynamics. Epilepsia. 1987;28(1):24-7. Doi:10.1111/j.1528-1157.1987.tb03617.x
122. Beelke M, Nobili L, Baglietto MG, et al. Relationship of sigma activity to sleep interictal epileptic discharges: a study in children affected by benign epilepsy with occipital paroxysms. Epilepsy Res. 2000;40(2-3):179-86.Doi:10.1016/s0920-1211(00)00131-5.
123. Nobili L, Ferrillo F, Baglietto MG, Beelke M, De Carli F, De Negri E, et al. Relationship of sleep interictal epileptiform discharges to sigma activity (12-16 Hz) in benign epilepsy of childhood with rolandic spikes. Clin Neurophysiol. 1999;110(1):39-46. Doi:10.1016/s0168-5597(98)00041-0.
124. Nobili L, Baglietto MG, Beelke M, De Carli F, De Negri E, Gaggero R, Rosadini G, Veneselli E, Ferrillo F. Distribution of epileptiform discharges during nREM sleep in the CSWSS syndrome: relationship with sigma and delta activities. Epilepsy Res. 2001;44(2-3):119-28. Doi:10.1016/s0920-1211(01)00191-7.
125. Ciumas C, Saignavongs M, Ilski F, et al. White matter development in children with benign childhood epilepsy with centro-temporal spikes. Brain. 2014;137(Pt 4):1095-106.
126. Bourel-Ponchel E, Mahmoudzadeh M, Berquin P, Wallois F. Local and Distant Dysregulation of Synchronization Around Interictal Spikes in BECTS. Front Neurosci. 2017;11:59. Doi:10.3389/fnins.2017.00059.
127. Shields W, Snead 3rd O. Benign epilepsy with centrotemporal spikes. Epilepsia. 2009;50:10-15. https://doi.org/10.1111/j.1528-1167.2009.02229.x
128. Rossi PG, Parmeggiani A, Bach V, Santucci M, Visconti P. EEG features and epilepsy in patients with autism. Brain Dev. 1995;17:169–74. 10.1016/0387-7604(95)00019-8.
129. Nass R, Devinsky O. Autistic regression with Rolandic spikes. Neuropsychiatry Neuropsychol Behav Neurol. 1999;12(3):193-7.
130. Holtmann M, Becker K, Kentner-Figura B, Schmidt MH. Increased frequency of Rolandic spikes in ADHD children. Epilepsia. 2003;44(9):1241.
131. Silvestri R, Gagliano A, Calarese T, et al. Ictal and interictal EEG abnormalities in ADHD children recorded over night by video-polysomnography. Epilepsy Res. 2007;75:130–7.
132. Danhofer P, Pejčochová J, Dušek L, Rektor I, Ošlejšková H. The influence of EEG-detected nocturnal centrotemporal discharges on the expression of core symptoms of ADHD in children with benign childhood epilepsy with centrotemporal spikes (BCECTS): A prospective study in a tertiary referral center. Epilepsy Behav. 2018;79:75-81. Doi:10.1016/j.yebeh.2017.11.007.
133. Kobayashi K, Yoshinaga H, Toda Y, Inoue T, Oka M, Ohtsuka Y. High-frequency oscillations in idiopathic partial epilepsy of childhood. Epilepsia. 2011;52(10):1812-9.Doi:10.1111/j.1528-1167.2011.03169.x
134. Tassinari CA, De Marco P, Plasmati R, Pantieri R, Blanco M, Michelucci R. Extreme somatosensory evoked potentials (ESEPs) elicited by tapping of hands or feet in children: a somatosensory cerebral evoked potentials study. Neurophysiol Clin. 1988;18(2):123-8. Doi:10.1016/s0987-7053(88)80117-5.
135. Ferri R, Del Gracco S, Elia M, Musumeci SA. Age-related changes of cortical excitability in subjects with sleep-enhanced centrotemporal spikes: a somatosensory evoked potential study. Clin Neurophysiol. 2000;111(4):591-9. Doi:10.1016/s1388-2457(99)00249-7
136. Shibasaki H, Yamashita Y, Neshige R, Tobimatsu S, Fukui R. Pathogenesis of giant somatosensory evoked potentials in progressive myoclonic epilepsy. Brain. 1985;108:225-40.
137. van Klink NE, van t Klooster MA, Leijten FS, Jacobs J, Braun KP, Zijlmans M. Ripples on Rolandic spikes: A marker of epilepsy severity. Epilepsia. 2016;57(7):1179-89. Doi:10.1111/epi.13423.
138. Fejerman N. Atypical rolandic epilepsy. Epilepsia 2009;50 Suppl 7:9-12.
139. Tovia E, Goldberg-Stern H, Ben Zeev B, et al. The prevalence of atypical presentations and comorbidities of benign childhood epilepsy with centrotemporal spikes. Epilepsia. 2011;52(8):1483-8. Doi:10.1111/j.1528-1167.2011.03136.x
140. Kramer U, Sagi L, Goldberg-Stern H, Zelnik N, Nissenkorn A, Ben-Zeev B. Clinical spectrum and medical treatment of children with electrical status epilepticus in sleep (ESES). Epilepsia. 2009;50(6):1517-24. Doi:10.1111/j.1528-1167.
141. Qian P, Li H, Xue J, Yang Z. Scalp-recorded high-frequency oscillations in atypical benign partial epilepsy. Clin Neurophysiol. 2016;127(10):3306-13. Doi:10.1016/j.clinph.2016.07.013
142. Fernandez S, Chapman KE. Peters JM, Kothare S, Nordli Jr DR. The tower of Babel: Survey on concepts and terminology in electrical status epilepticus in sleep and continuous spikes and waves during sleep in North America. Epilepsia. 2013;54(4):741-50. Doi:10.1111/epi.12039
143. Patry G, Lyagoubi S, Tassinari CA. Subclinical electrical status epilepticus induced by sleep in children. Arch Neurol. 1971;24:242–52. 10.1001/archneur.1971.00480330070006
144. Tassinari CA, Rubboli G, Volpi L, et al. Encephalopathy with electrical status epilepticus during slow sleep or ESES syndrome including the acquired aphasia. Clin Neurophysiol. 2000;111 Suppl 2:S94-S102. Doi:10.1016/s1388-2457(00)00408-9.
145. Tassinari CA, Cantalupo G, Rios-Pohl L, Giustina ED, Rubboli G. Encephalopathy with status epilepticus during slow sleep: “the Penelope syndrome”. Epilepsia. 2009;50 Suppl 7:4–8
146. Kellermann K. Recurrent aphasia with subclinical bioelectric status epilepticus during sleep. Eur J Pediatrics. 1978;128:207–12.
147. Parisi P, Spalice A, Nicita F, et al. Epileptic encephalopathy of infancy and childhood: electro-clinical pictures and recent understandings. Curr. Neuropharmacol. 2010;8:409-21.
148. Metz-Lutz MN, Filippini M. Neuropsychological findings in Rolandic epilepsy and Landau-Kleffner syndrome. Epilepsia. 2006;47 Suppl 2:71-5. Doi:10.1111/j.1528-1167.2006.00695.x.
149. Dulac O. Epileptic encephalopathy. Epilepsia. 2001;42 Suppl 3:23-6.
150. Deonna T, Roulet-Perez E. Early-onset acquired epileptic aphasia (Landau-Kleffner syndrome, LKS) and regressive autistic disorders with epileptic EEG abnormalities: the continuing debate. Brain Dev. 2010;32:746–52
151. Guliyeva U, Nino Tatishvili N, Kaiyrzhanov R. Rolandic Epilepsy: Self-Limited Epilepsy with Centrotemporal Spikes. Epilepsy - Update on Classification, Etiologies, Instrumental Diagnosis and Treatment. IntechOpen; 2021. Available from: http://dx.doi.org/10.5772/intechopen.96148.
152. Overvliet GM, Besseling RM, Jansen JF, et al. Early onset of cortical thinning in children with rolandic epilepsy. Neuroimage Clin. 2013;2:434-9. Doi:10.1016/j.nicl.2013.03.008.):8-16. Doi:https://doi.org/10.1111/epi.17241
153. Ellenrieder N, Dubeau F, Gotman J, Frauscher B. Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties. Neuroimage Clin. 2017;14:566-573. Doi:10.1016/j.nicl.2017.02.018
154. Koutroumanidis M, Panayiotopoulos CP. Benign childhood seizure susceptibility syndromes. In: Rugg-Gunn RJ, Smalls JE, editors. From channels to commissioning – a practical guide to epilepsy. London: International League Against Epilepsy (UK Chapter and Epilepsy Society; 2015. Pp:89-113).
155. Wolf P. Reading epilepsy. In J Roger, M Bureau, C Dravet, FE Dreifuss, A Perret, P Wolf (Eds). Epileptic syndromes in infancy, childhood and adolescence. 2nd ed. John Libbey, 1992 London, pp:281–98.
156. Puteikis K, Mameniškienė R, Wolf P. Reading epilepsy today: A scoping review and meta-analysis of reports of the last three decades. Epilepsy Behav. 2023;145:109346. Doi:10.1016/j.yebeh.2023.109346.
157. Valenti MP, Tinuper P, Cerullo A, Carcangiu R, Marini C. Reading epilepsy in a patient with previous idiopathic focal epilepsy with centrotemporal spikes. Epileptic Disord. 1999;1(3):167-71
158. Wolf P. Reflex epileptic mechanisms in humans: Lessons about natural ictogenesis. Epilepsy Behav. 2017;71(Pt B):118-123. Doi:10.1016/j.yebeh.2015.01.009
159. Geschwind N, Sherwin I. Language-induced epilepsy. Arch Neurol. 1967;16:25–31.
160. Lee SI, Sutherling WW, Persing JA, Butler AB. Language induced seizure: a case of cortical origin. Arch Neurol.1980;37:433–6.
161. Tanaka N, Sakurai K, Kamada K, Takeuchi F, Takeda Y, Koyama T. Neuromagnetic source localization of epileptiform activity in patients with graphogenic epilepsy. Epilepsia. 2006;47(11):1963-7.
162. Cirignotta F, Zucconi M, Mondini S, Lugaresi E. Writing epilepsy. Clin Electroencephalogr. 1985;17(1):21-3.
163. Chifari R, Piazzini A, Turner K, Canger R, Canevini MP, Wolf P. Reflex writing seizures in two siblings with juvenile myoclonic epilepsy. Acta Neuro Scand. 2004;109:232–5.
164. Oshima T, Hirose K, Murakami H, Suzuki S, Kanemoto K. Graphogenic epilepsy: a variant of language-induced epilepsy distinguished form reading- and praxis-induced epilepsy. Seizure. 2003;12:56–9.
165. Rutherling WW, Hershman LM, Miller JQ, Lee SI. Seizures induced by playing music. Neurology. 1980;30(9):1001-4. Doi:10.1212/wnl.30.9.1001
166. Herskowitz J, Rosman NP, Geschwind N. Seizures induced by singing and recitation. A unique form of reflex epilepsy in childhood. Arch Neurol. 1984;41(10):1102-3.
167. Critchley M. Musicogenic epilepsy. In: M Critchley, RA Hensen, eds. Music and the Brain London: Heinemann, 1977:344–53.
168. Avanzini G. Musicogenic seizures. Ann NY Acad Sci. 2003;999(1):95.
169. Nuara A, Mirandola L, Fabbri-Destro M, et al. Spatio-temporal dynamics of interictal activity in musicogenic epilepsy: Two case reports and a systematic review of the literature. Clin Neurophysiol. 2020;131(10):2393- 2401. Doi:10.1016/j.clinph.2020.06.028
170. Bratu IF, Nica AE, Oane I, et al. Musicogenic seizures in temporal lobe epilepsy: Case reports based on ictal source localization analysis. Front Neurol. 2023;14:1072075..
171. Pittau F, Tinuper P, Bisulli F, et al. Videopolygraphic and functional MRI study of musicogenic epilepsy. A case report and literature review. Epilepsy Behav. 2008;13(4):685-92. Doi:10.1016/j.yebeh.2008.05.004.
172. Wieser HG, Hungerbühler H, Siegel AM, Buck A. Musicogenic epilepsy: review of the literature and case report with ictal single photon emission computed tomography. Epilepsia. 1997;38(2):200-7.
173. Cho JW, Seo DW, Joo EY, Tae W S, Lee J, Hong SB. Neural correlates of musicogenic epilepsy: SISCOM and FDG-PET. Epilepsy Res. 2007;77(2-3):169-73.
174. Hauser WA, Annegers JF, Kurland LT. Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota. Epilepsia. 1993;34:453–68.
175. Frey LC. Epidemiology of posttraumatic epilepsy: a critical review. Epilepsia. 2003;44(s10):11-7
176. Echlin FA, Arnett V, Zoll J. Paroxysmal high voltage discharges from isolated and partially isolated human and animal cerebral cortex. Electroencephalogr Clin Neurophysiol. 1952;4(2):147-64. Doi:10.1016/0013-4694(52)90004-7.
177. Houweling AR, Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. Homeostatic synaptic plasticity can explain post-traumatic epileptogenesis in chronically isolated neocortex. Cereb Cortex. 2005;15(6):834-45.. Doi:10.1093/cercor/bhh184.
178. Avramescu S, Timofeev I. Synaptic Strength Modulation After Cortical Trauma: A Role in Epileptogenesis. J Neurosci. 2008;28(27):6760-72.
179. Massimini M, Corbetta M, Sanchez-Vives MV, et al. Sleep-like cortical dynamics during wakefulness and their network effects following brain injury. Nature Communications. 2024;15:7207. https://doi.org/10.1038/s41467-024-51586-1.