Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Current Neurology and Neuroscience Reports
Published in: Current Neurology and Neuroscience Reports 9/2023

17-07-2023 | Epilepsy

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

Authors: Annie H. Roliz, Sanjeev Kothare

Published in: Current Neurology and Neuroscience Reports | Issue 9/2023

Login to get access

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.

Summary

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.
Literature
1.
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.CrossRef
3.
Kotagal P, Yardi N. The relationship between sleep and epilepsy. Semin Pediatr Neurol. 2008;15:42–9.PubMedCrossRef
4.
Kumar P, Rajar TR. Seizure susceptibility decreases with enhancement of rapid eye movement sleep. Brain Res. 2001;922:299–304.PubMedCrossRef
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.PubMedCrossRef
6.
Roliz AH, Kothare S. The interaction between sleep and epilepsy. Curr Neurol Neurosci Rep. 2022;22:551–63.PubMedCrossRef
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.PubMedCrossRef
8.
Bourel-ponchel E, Hasaerts D. Behavioral-state development and sleep-state differentiation during early ontogenesis. Neurophysiol Clin / Clin Neurophysiol. 2021;51:89–98.CrossRef
9.
10.
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.PubMedCrossRef
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.PubMedCrossRef
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.CrossRef
14.
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
20.
Freudigman KA, Thoman EB. Infant sleep during the first postnatal day: an opportunity for assessment of vulnerability. Pediatrics. 1993;92(3):373–9.PubMed
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.CrossRef
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.CrossRef
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.PubMedCrossRef
24.
Halász P, Szűcs A. Sleep and epilepsy link by plasticity. Front Neurol. 2020;11:1–25.CrossRef
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.PubMedPubMedCentralCrossRef
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.CrossRef
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.PubMedCrossRef
31.
32.
Tononi G, Cirelli C. Sleep and the price of plasticity. Neuron. 2014;23:1–7.
33.
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.PubMedPubMedCentralCrossRef
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.PubMedPubMedCentralCrossRef
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.PubMedCrossRef
37.
38.
Lignani G, Baldelli P, Marra V. Homeostatic plasticity in epilepsy. Front Cell Neurosci. 2020;14:1–9.CrossRef
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.CrossRef
40.
Frank MG. Erasing synapses in sleep: is it time to be SHY? Neural Plast. 2012;2012:1–25.CrossRef
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.PubMedCrossRef
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.PubMedPubMedCentralCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.CrossRef
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.PubMedPubMedCentralCrossRef
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.CrossRef
51.
Schiller K. Focal epilepsy impacts rapid eye movement sleep microstructure. Sleep. 2023;46:1–12.CrossRef
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.PubMedPubMedCentralCrossRef
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.PubMedPubMedCentralCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.CrossRef
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.CrossRef
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.PubMedCrossRef
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.CrossRef
62.
Rossi KC, Joe J, Makhija MGD. Insufficient sleep, electroencephalogram activation, and seizure risk: re-evaluating the evidence. Ann Neurol. 2020;87:798–806.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedPubMedCentralCrossRef
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.PubMedCrossRef
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.CrossRef
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.PubMedPubMedCentralCrossRef
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.PubMedCrossRef
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.CrossRef
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.PubMedCrossRef
73.
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
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.PubMedCrossRef
78.
Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14:540–5.PubMedCrossRef
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.PubMed
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.PubMedPubMedCentralCrossRef
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.PubMedPubMedCentralCrossRef
82.
Chung F, Yegneswaran B, Liao P, Chung SA, Vairavanathan S, Islam S, et al. STOP questionnaire. Anesthesiology. 2008;108:812–21.PubMedCrossRef
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.PubMedPubMedCentralCrossRef
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.PubMedCrossRef
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.
Metadata
Title
The Relationship Between Sleep, Epilepsy, and Development: a Review
Authors
Annie H. Roliz
Sanjeev Kothare
Publication date
17-07-2023
Publisher
Springer US
Published in
Current Neurology and Neuroscience Reports / Issue 9/2023
Print ISSN: 1528-4042
Electronic ISSN: 1534-6293
DOI
https://doi.org/10.1007/s11910-023-01284-0

Other articles of this Issue 9/2023

Current Neurology and Neuroscience Reports 9/2023 Go to the issue

Review

Polypharmacy in multiple sclerosis

ReviewPaper

A Clinical Approach to Existing and Emerging Therapeutics in Neuromyelitis Optica Spectrum Disorder

Review

Hematopoietic stem cell transplantation for MS

Review

Cognitive interventions for neurodegenerative disease

ReviewPaper

Measuring Pathology in Patients with Multiple Sclerosis Using Positron Emission Tomography

Review

Trigeminal autonomic cephalalgias and neuralgias in children and adolescents
Image Credits