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Current neurology and neuroscience reports
09, 2023;23 (9): 469-477.

The Relationship Between Sleep, Epilepsy, and Development: a Review.

Annie H Roliz, Sanjeev Kothare
Author Information
  1. Annie H Roliz: Division of Child Neurology, Department of Pediatrics, Cohen Children's Medical Center, 2001 Marcus Ave, Suite W290, New Hyde Park, NY, 11042, USA.
  2. Sanjeev Kothare: Division of Child Neurology, Department of Pediatrics, Cohen Children's Medical Center, 2001 Marcus Ave, Suite W290, New Hyde Park, NY, 11042, USA. skothare@northwell.edu.
PMID: 37458984 DOI: 10.1007/s11910-023-01284-0

Abstract

PURPOSE OF REVIEW: To review the relationship between sleep, neurodevelopment, and Epilepsy and potential underlying physiological mechanisms.
RECENT FINDINGS: Recent studies have advanced our understanding of the role of sleep in early brain development and Epilepsy. Epileptogenesis has been proposed to occur when there is a failure of normal adaptive processes of synaptic and homeostatic plasticity. This sleep-dependent transformation may explain the cognitive impairment seen in Epilepsy, especially when occurring early in life. The glymphatic system, a recently discovered waste clearance system of the central nervous system, has been described as a potential mechanism underlying the relationship between sleep and seizures and may account for the common association between sleep deprivation and increased seizure risk. Epilepsy and associated sleep disturbances can critically affect brain development and neurocognition. Here we highlight recent findings on this topic and emphasize the importance of screening for sleep concerns in people with Epilepsy.

Keywords

Epilepsy Glymphatic system Homeostatic plasticity Sleep Sleep deprivation Synaptic homeostasis

References

  1. Mukai Y, Yamanaka A. Functional roles of REM sleep. Neurosci Res. 2023;189:44–53. [PMID: 36572254]
  2. Ng M, Pavlova M. Why are seizures rare in rapid eye movement sleep? Review of the frequency of seizures in different sleep stages. Epilepsy Res Treat. 2013;2013:1–10. [DOI: 10.1155/2013/932790]
  3. Kotagal P, Yardi N. The relationship between sleep and epilepsy. Semin Pediatr Neurol. 2008;15:42–9. [PMID: 18555190]
  4. Kumar P, Rajar TR. Seizure susceptibility decreases with enhancement of rapid eye movement sleep. Brain Res. 2001;922:299–304. [PMID: 11743963]
  5. Knoop MS, De Groot ER, Dudink J. Current ideas about the roles of rapid eye movement and non–rapid eye movement sleep in brain development. Acta Paediatr. 2021;110:36–44. [PMID: 32673435]
  6. Roliz AH, Kothare S. The interaction between sleep and epilepsy. Curr Neurol Neurosci Rep. 2022;22:551–63. [PMID: 35802300]
  7. Vecchierini M-F, D’Allest A-M, Verpellat P. EEG patterns in 10 extreme premature neonates with normal neurological outcome: qualitative and quantitative data. Brain Dev. 2003;25:330–7. [PMID: 12850512]
  8. Bourel-ponchel E, Hasaerts D. Behavioral-state development and sleep-state differentiation during early ontogenesis. Neurophysiol Clin / Clin Neurophysiol. 2021;51:89–98. [DOI: 10.1016/j.neucli.2020.10.003]
  9. Roffwarg HP, Muzio JN, Dement WC. Ontogenetic development of the human sleep-dream cycle. Published by: American Association for the Advancement of Science Stable URL: https://www.jstor.org/stable/1718980 . 1966;152:604–19.
  10. Lokhandwala S, Spencer RMC. Relations between sleep patterns early in life and brain development: a review. Dev Cogn Neurosci. 2022;56:101130. [PMID: 35779333]
  11. Ravassard P, Hamieh AM, Joseph MA, Fraize N, Libourel PA, Lebarillier L, et al. REM sleep-dependent bidirectional regulation of hippocampal-based emotional memory and LTP. Cereb Cortex. 2016;26:1488–500. [PMID: 25585510]
  12. Ishikawa A, Kanayama Y, Matsumura H, Tsuchimochi H, Ishida Y, Nakamura S. Selective rapid eye movement sleep deprivation impairs the maintenance of long-term potentiation in the rat hippocampus. Eur J Neurosci. 2006;24:243–8. [PMID: 16882020]
  13. Zhou Y, Lai CSW, Bai Y, Li W, Zhao R, Yang G, et al. REM sleep promotes experience-dependent dendritic spine elimination in the mouse cortex. Nat Commun. 2020;11:1–12. [DOI: 10.1038/s41467-020-18592-5]
  14. Li W, Ma L, Yang G, Gan WB. REM sleep selectively prunes and maintains new synapses in development and learning. Nat Neurosci. 2017;20:427–37. [PMID: 28092659]
  15. Shaffery JP, Lopez J, Bissette G, Roffwarg HP. Rapid eye movement sleep deprivation in post-critical period, adolescent rats alters the balance between inhibitory and excitatory mechanisms in visual cortex. Neurosci Lett. 2006;393:131–5. [PMID: 16236445]
  16. Buchmann A, Ringli M, Kurth S, et al. EEG sleep slow-wave activity as a mirror of cortical maturation. Cereb Cortex. 2011;21(3):607–15. [PMID: 20624840]
  17. Chan M, Wong TCH, Weichard A, Nixon GM, Walter LM, Horne RSC. Sleep macro-architecture and micro-architecture in children born preterm with sleep disordered breathing. Pediatr Res. 2020;87:703–10. [PMID: 31195406]
  18. Perkinson-gloor N, Arx PH, Brand S, Holsboer-trachsler E, Grob A, Weber P, et al. The role of sleep and the hypothalamic-pituitary-adrenal axis for behavioral and emotional problems in very preterm children during middle childhood. J Psychiatr Res. 2015;60:141–7. [PMID: 25454023]
  19. Lopez J, Roffwarg HP, Dreher A, Bissette G, Karolewicz B, Shaffery JP. Rapid eye movement sleep deprivation decreases long-term potentiation stability and affects some glutamatergic signaling proteins during hippocampal development. Neuroscience. 2008;153:44–53. [PMID: 18359575]
  20. Freudigman KA, Thoman EB. Infant sleep during the first postnatal day: an opportunity for assessment of vulnerability. Pediatrics. 1993;92(3):373–9. [PMID: 7689726]
  21. Shellhaas RA, Burns JW, Hassan F, Carlson MD, Barks JDE, Chervin RD. Neonatal sleep-wake analyses predict 18-month neurodevelopmental outcomes. Sleep. 2017;40:1–9. [DOI: 10.1093/sleep/zsx144]
  22. Bijlsma A, Beunders VAA, Dorrepaal DJ, Joosten KFM, van Beijsterveldt IALP, Dudink J, et al. Sleep and 24-hour rhythm characteristics in preschool children born very-preterm and full-term. J Clin Sleep Med. 2023;19:639–40. [DOI: 10.5664/jcsm.10408]
  23. Morse AM, Kothare SV. Does sleep correlate with neurodevelopmental outcomes in preterm and term infants in early-preschool children? J Clin Sleep Med. 2023;19:639–40. [PMID: 36798981]
  24. Halász P, Szűcs A. Sleep and epilepsy link by plasticity. Front Neurol. 2020;11:1–25. [DOI: 10.3389/fneur.2020.00911]
  25. Steriade M. Neuronal substrates of sleep and epilepsy. Cambridge: Cambridge University Press; 2003.
  26. Hebbes D. The organization of behavior. New York: Wiley; 1949.
  27. Bliss TVP, Gardner-Medwin AR. Long-lasting potentiation of synaptic transmission in the dentate area of the unanaesthetized rabbit following stimulation of the perforant path. J Physiol. 1973;232:357–74. [PMID: 4727085]
  28. Kuhn M, Wolf E, Maier JG, Mainberger F, Feige B, Schmid H, et al. Sleep recalibrates homeostatic and associative synaptic plasticity in the human cortex. Nat Commun. 2016;7:1–9. [DOI: 10.1038/ncomms12455]
  29. Arshavsky YI. Memory: synaptic or cellular, that is the question. Neurosci. 2022;00:1–16.
  30. Issa NP, Nunn KC, Wu S, Haider HA, Tao JX. Putative roles for homeostatic plasticity in epileptogenesis. Epilepsia. 2023;64:539–52. [PMID: 36617338]
  31. Tononi G, Cirelli C. Sleep function and synaptic homeostasis. Sleep Med Rev. 2006;10:49–62. [PMID: 16376591]
  32. Tononi G, Cirelli C. Sleep and the price of plasticity. Neuron. 2014;23:1–7.
  33. Bushey D, Tononi G, Cirelli C. Sleep and synaptic homeostasis: structural evidence in Drosophila. Science. 2011;332:1576–81. [PMID: 21700878]
  34. Maret S, Faraguna U, Nelson AB, Cirelli C, Tononi G. Sleep and waking modulate spine turnover in the adolescent mouse cortex. Nat Neurosci. 2011;14:1418–20. [PMID: 21983682]
  35. Yang G, Gan WB. Sleep contributes to dendritic spine formation and elimination in the developing mouse somatosensory cortex. Dev Neurobiol. 2012;72:1391–8. [PMID: 22058046]
  36. Ghilardi M, Ghez C, Dhawan V, Moeller J, Mentis M, Nakamura T, et al. Patterns of regional brain activation associated with different forms of motor learning. Brain Res. 2000;871:127–45. [PMID: 10882792]
  37. Huber R, Ghilardi MF, Massimini M, Tononi G. Local sleep and learning. Nature. 2004;430:78–81. [PMID: 15184907]
  38. Lignani G, Baldelli P, Marra V. Homeostatic plasticity in epilepsy. Front Cell Neurosci. 2020;14:1–9. [DOI: 10.3389/fncel.2020.00197]
  39. Canet E, Gaultier C, D’Allest A, Dehan M. Effects of sleep deprivation on respiratory events during sleep in healthy infants. J Appl Physiol. 1979;66:1158–63. [DOI: 10.1152/jappl.1989.66.3.1158]
  40. Frank MG. Erasing synapses in sleep: is it time to be SHY? Neural Plast. 2012;2012:1–25. [DOI: 10.1155/2012/264378]
  41. Zanzmera P, Shukla G, Gupta A, Singh H, Goyal V, Srivastava A, et al. Markedly disturbed sleep in medically refractory compared to controlled epilepsy - a clinical and polysomnography study. Seizure. 2012;21:487–90. [PMID: 22633696]
  42. Calvello C, Fernandes M, Lupo C, Maramieri E, Placidi F, Izzi F, et al. Sleep architecture in drug-naïve adult patients with epilepsy: comparison between focal and generalized epilepsy. Epilepsia Open. 2023;8:165–72. [PMID: 36529529]
  43. Winsor AA, Richards C, Bissell S, Seri S, Liew A, Bagshaw AP. Sleep disruption in children and adolescents with epilepsy: a systematic review and meta-analysis. Sleep Med Rev. 2021;57:101416. [PMID: 33561679]
  44. Manokaran RK, Tripathi M, Chakrabarty B, Pandey RM, Gulati S. Sleep abnormalities and polysomnographic profile in children with drug-resistant epilepsy. Seizure. 2020;82:59–64. [PMID: 33011589]
  45. Pereira AM, Bruni O, Ferri R, Palmini A, Nunes ML. The impact of epilepsy on sleep architecture during childhood. Epilepsia. 2012;53:1519–25. [PMID: 22709355]
  46. Yeh WC, Lai CL, Wu MN, Lin HC, Lee KW, Li YS, et al. Rapid eye movement sleep disturbance in patients with refractory epilepsy: a polysomnographic study. Sleep Med. 2021;81:101–8. [PMID: 33647761]
  47. Mekky JF, Elbhrawy SM, Boraey MF, Omar HM. Sleep architecture in patients with juvenile myoclonic epilepsy. Sleep Med Elsevier Ltd. 2017;38:116–21. [DOI: 10.1016/j.sleep.2017.02.013]
  48. Scarlatelli-Lima AV, Sukys-Claudino L, Watanabe N, Guarnieri R, Walz R, Lin K. How do people with drug-resistant mesial temporal lobe epilepsy sleep? A clinical and video-EEG with EOG and submental EMG for sleep staging study. eNeurologicalSci. 2016;4:34–41. [PMID: 29430547]
  49. Ikoma Y, Takahashi Y, Sasaki D, Matsui K. Properties of REM sleep alterations with epilepsy. Brain. 2023;00:1–12.
  50. Sadak U, Honrath P, Ermis U, Heckelmann J, Meyer T, Weber Y, et al. Reduced REM sleep: a potential biomarker for epilepsy – a retrospective case-control study. Seizure Elsevier Ltd. 2022;98:27–33. [DOI: 10.1016/j.seizure.2022.03.022]
  51. Schiller K. Focal epilepsy impacts rapid eye movement sleep microstructure. Sleep. 2023;46:1–12. [DOI: 10.1093/sleep/zsac250]
  52. Schiller K, Avigdor T, Abdallah C, Sziklas V, Crane J, Stefani A, et al. Focal epilepsy disrupts spindle structure and function. Sci Rep. 2022;12:11137. [PMID: 35778434]
  53. Oyegbile-chidi T, Harvey D, Dunn D, Jones J, Hermann B, Byars A, et al. Pediatric neurology characterizing sleep phenotypes in children with newly diagnosed epilepsy. Pediatr Neurol. 2022;137:34–40. [PMID: 36215818]
  54. Jethwa S, Pressler RM, Kaya D, Datta AN. Sleep architecture in neonatal and infantile onset epilepsies in the first six months of life: a scoping review. Eur J Paediatr Neurol. 2022;41:99–108. [PMID: 36410286]
  55. Tassinari CA, Rubboli G. Encephalopathy related to status epilepticus during slow sleep: current concepts and future directions. Epileptic Disord. 2019;21:S82–7.
  56. Rubboli G, Gardella E, Cantalupo G, Tassinari C. Encephalopathy related to status epilepticus during slow sleep (ESES): pathophysiological insights and nosological considerations. Epilepsy Behav. 2023;140:109105. [PMID: 36758358]
  57. Proost R, Lagae L, Van Paesschen W, Jansen K. Sleep in children with refractory epilepsy and epileptic encephalopathies: a systematic review of literature. Eur J Paediatr Neurol Elsevier Ltd. 2022;38:53–61. [DOI: 10.1016/j.ejpn.2022.03.010]
  58. Frucht MM, Quigg M, Schwaner C, Fountain NB. Distribution of seizure precipitants among epilepsy syndromes. 2000;41:1534–9.
  59. Dinner D. Effect of sleep on epilepsy. J Clin Neurophysiol. 2022;19:504–13. [DOI: 10.1097/00004691-200212000-00003]
  60. Rowan AJ, Veldhuisen RJ, Nagelkerke NJ. Comparative evaluation of sleep deprivation and sedated sleep EEGs as diagnostic aids in epilepsy. Electroencephalogr Clin Neurophysiol. 1982;54:357–64. [PMID: 6181958]
  61. Degen R. A study of the diagnostic value of waking and sleep EEGs after sleep deprivation in epileptic patients on anticonvulsive therapy. Clin Neurophysiol. 1980;49:577–84. [DOI: 10.1016/0013-4694(80)90398-3]
  62. Rossi KC, Joe J, Makhija MGD. Insufficient sleep, electroencephalogram activation, and seizure risk: re-evaluating the evidence. Ann Neurol. 2020;87:798–806. [PMID: 32118310]
  63. Díaz-Negrillo A. Influence of sleep and sleep deprivation on ictal and interictal epileptiform activity. Epilepsy Res Treat. 2013;2013.
  64. Malow BA, Passaro E, Milling C, Minecan DN, Levy K. Sleep deprivation does not affect seizure frequency during inpatient video-EEG monitoring. Neurology. 2002;59(9):1371–4. [PMID: 12427886]
  65. Cobabe MM, Sessler DI, Nowacki AS, Rourke CO, Andrews N, Foldvary-schaefer N. Impact of sleep duration on seizure frequency in adults with epilepsy: a sleep diary study. Epilepsy Behav. 2015;43:143–8. [PMID: 25623812]
  66. Dell KL, Payne DE, Kremen V, Maturana MI, Gerla V, Nejedly P, et al. Seizure likelihood varies with day-to-day variations in sleep duration in patients with refractory focal epilepsy: a longitudinal electroencephalography investigation. EClinicalMedicine. 2021;37:100934. [PMID: 34386736]
  67. Stirling RE, Hidajat CM, Grayden DB, et al. Sleep and seizure risk in epilepsy: bed and wake times are more important than sleep duration. Brain. 2023;146(7):2803–13. [PMID: 36511881]
  68. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, et al. A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med. 2012;4:1–22. [DOI: 10.1126/scitranslmed.3003748]
  69. Iliff JJ, Chen MJ, Plog BA, Zeppenfeld DM, Soltero M, Yang L, et al. Impairment of glymphatic pathway function promotes tau pathology after traumatic brain injury. J Neurosci. 2014;34:16180–93. [PMID: 25471560]
  70. Christensen J, Yamakawa GR, Shultz SR, Mychasiuk R. Is the glymphatic system the missing link between sleep impairments and neurological disorders? Examining the implications and uncertainties. Prog Neurobiol. 2020;198:101917. [PMID: 32991958]
  71. Bishir M, Bhat A, Essa MM, Ekpo O, Ihunwo AO, Veeraraghavan VP, et al. Sleep deprivation and neurological disorders. Biomed Res Int. 2020;2020:1–19. [DOI: 10.1155/2020/5764017]
  72. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, et al. Sleep drives metabolite clearance from the adult brain. Science. 2013;342:373–7. [PMID: 24136970]
  73. Jessen NA, Munk ASF, Lundgaard I, Nedergaard M. The glymphatic system: a beginner’s guide. Neurochem Res. 2015;40:2583–99. [PMID: 25947369]
  74. Mehta A, Prabhakar M, Kumar P, Deshmukh R, Sharma PL. Excitotoxicity: bridge to various triggers in neurodegenerative disorders. Eur J Pharmacol. 2013;698:6–18. [PMID: 23123057]
  75. Rabinovitch A, Aviramd I, Biton Y, Braunstein D. A combined astrocyte – G-lymphatic model of epilepsy initiation, maintenance and termination. Med Hypotheses. 2019;133:109384. [PMID: 31494484]
  76. Hadaczek P, Yamashita Y, Mirek H, Noble C, Park J, Bankiewicz K. The, “perivascular pump” driven by arterial pulsation is a powerful mechanism for the distribution of therapeutic molecules. Mol Ther. 2006;14:69–78. [PMID: 16650807]
  77. Buysse DJ, Reynolds CF III, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28:193–213. [PMID: 2748771]
  78. Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14:540–5. [PMID: 1798888]
  79. Drake C, Nickel C, Burduvali E, Roth T, Jefferson C, Badia P. The pediatric daytime sleepiness scale (PDSS): sleep habits and school outcomes in middle-school children. Sleep. 2003;26:455–8. [PMID: 12841372]
  80. Spilsbury JC, Drotar D, Rosen CL, Redline S. The Cleveland Adolescent Sleepiness Questionnaire: a new measure to assess excessive daytime sleepiness in adolescents. J Clin Sleep Med. 2007;3:603–12. [PMID: 17993042]
  81. Yu JL, Rosen I. Utility of the modified Mallampati grade and Friedman tongue position in the assessment of obstructive sleep apnea. J Clin Sleep Med. 2020;16:303–8. [PMID: 31992434]
  82. Chung F, Yegneswaran B, Liao P, Chung SA, Vairavanathan S, Islam S, et al. STOP questionnaire. Anesthesiology. 2008;108:812–21. [PMID: 18431116]
  83. Chung F, Subramanyam R, Liao P, Sasaki E, Shapiro C, Sun Y. High STOP-Bang score indicates a high probability of obstructive sleep apnoea. Br J Anaesth. 2012;108:768–75. [PMID: 22401881]
  84. Chervin RD. Pediatric sleep questionnaire (PSQ): validity and reliability of scales for sleep-disordered breathing, snoring, sleepiness, and behavioral problems. Sleep Med. 2000;1:21–32. [PMID: 10733617]
  85. Shahid A, Wilkinson K, Marcu S, Shapiro CM. STOP. THAT and one hundred other sleep scales. STOP: THAT one hundred other sleep scales; 2012. p. 1–406.

MeSH Term

Humans
Epilepsy
Sleep
Seizures
Sleep Deprivation
Homeostasis
Journal Article Review
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