Maternal Methyl-Enriched Diet Normalizes Characteristics of the Sleep–Wake Cycle and Sleep Spindles in Adult Offspring of WAG/Rij Rats with Genetic Absence Epilepsy

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It has been previously shown that the perinatal maternal methyl-enriched diet (MED) reduces the number of spike-wave discharges (SWDs) and behavioral symptoms of depression in the adult offspring of WAG/Rij rats. Epilepsy and depression are usually accompanied by disturbances in the sleep-wake cycle. SWDs and sleep spindles are different manifestations of thalamocortical activity It is assumed that pathological alterations in the thalamocortical system that lead to SWD also change the sleep spindles. It is possible that the maternal MED has a positive effect not only on the SWD, but also on the sleep spindles. The purpose of this work is to find out whether maternal MED affects the sleep-wake cycle and whether it changes the characteristics of sleep spindles in adult offspring of WAG/Rij rats. It has been shown that in the offspring of WAG/Rij rats born to mothers who consumed MED during the perinatal period compared to the offspring whose mothers consumed control diet (CD), the relative duration of REM sleep significantly increases. In the offspring of WAG/Rij rats whose mothers consumed MED, the relative duration of REM sleep and the number of its episodes become indistinguishable from those in non-epileptic Wistar rats. Maternal MED also increases the number of transitions from slow-wave to REM sleep. There is a significant negative correlation between the number of SWDs and the duration of REM sleep. Maternal MED compare to CD decreased the amplitude and spectral power density of sleep spindles. They became much closer to the amplitude and spectral power of density of sleep spindles in Wistar rats. Thus, maternal MED normalizes characteristics of the sleep-wake cycle and sleep spindles in adult offspring of WAG/Rij rats. We hypothesize that this positive effect is associated with a reduction in the symptoms of absence epilepsy and comorbid depression, as well as with the correction of the activity of the thalamocortical system.

作者简介

A. Gabova

Institute of Higher Nervous Activity and Neurophysiology of RAS

编辑信件的主要联系方式.
Email: agabova@yandex.ru
Russia, Moscow

K. Sarkisova

Institute of Higher Nervous Activity and Neurophysiology of RAS

Email: agabova@yandex.ru
Russia, Moscow

参考

  1. Sarkisova K, van Luijtelaar G (2011) The WAG/Rij strain: A genetic animal model of absence epilepsy with comorbidity of depressiony. Prog Neuro-Psychopharmacol Biol Psychiatry 35: 854–876. https://doi.org/10.1016/j.pnpbp.2010.11.010
  2. Kobow K, Blümcke I (2012) The emerging role of DNA methylation in epileptogenesis. Epilepsia 53: 11–20. https://doi.org/10.1111/epi.12031
  3. Vialou V, Feng J, Robison AJ, Nestler EJ (2013) Epigenetic mechanisms of depression and antidepressant action. Annu Rev Pharmacol Toxicol 53: 59–87. https://doi.org/10.1146/annurev-pharmtox-010611-134540
  4. Sarkisova KY, Gabova AV, Fedosova EA, Shatskova AB (2020) Gender-dependent effect of maternal methyl-enriched diet on the expression of genetic absence epilepsy and comorbid depression in adult offspring of WAG/Rij Rats. Dokl Biol Sci 494: 244–247. https://doi.org/10.1134/S0012496620050075
  5. Lahtinen A, Puttonen S, Vanttola P, Viitasalo K, Sulkava S, Pervjakova N, Joensuu A, Salo P, Toivola A, Härmä M, Milani L, Perola M, Paunio T (2019) A distinctive DNA methylation pattern in insufficient sleep. Sci Rep 9: 1–9. https://doi.org/10.1038/s41598-018-38009-0
  6. Colavito V, Fabene PF, Grassi–Zucconi G, Pifferi F, Lamberty Y, Bentivoglio M, Bertini G (2013) Experimental sleep deprivation as a tool to test memory deficits in rodents. Front Syst Neurosci 7: 1–17. https://doi.org/10.3389/fnsys.2013.00106
  7. Kansagra S (2020) Sleep disorders in adolescents. Pediatrics 145(Suppl 2): S204–S209. https://doi.org/10.1542/PEDS.2019-2056I
  8. Fogel SM, Smith CT (2011) The function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation. Neurosci Biobehav Rev 35: 1154–1165. https://doi.org/10.1016/j.neubiorev.2010.12.003
  9. Al-Biltagi MA (2014) Childhood epilepsy and sleep. World J Clin Pediatr 3: 45. https://doi.org/10.5409/wjcp.v3.i3.45
  10. Dinopoulos A, Tsirouda MA, Bonakis A, Pons R, Pavlopoulou ID, Tsoumakas K (2018) Sleep architecture and epileptic characteristics of drug naïve patients in childhood absence epilepsy spectrum. A prospective study. Seizure 59: 99–107. https://doi.org/10.1016/j.seizure.2018.04.021
  11. Gandolfo G, Romettino S, Gottesmann C, Van Luijtelaar G, Coenen A (1990) Genetically epileptic rats show a pronounced intermediate stage of sleep. Physiol Behav 47: 213–215. https://doi.org/10.1016/0031-9384(90)90063-A
  12. van Luijtelaar G, Bikbaev A (2007) Midfrequency cortico-thalamic oscillations and the sleep cycle: Genetic, time of day and age effects. Epilepsy Res 73: 259–265. https://doi.org/10.1016/j.eplepsyres.2006.11.002
  13. Sitnikova E (2021) Sleep disturbances in rats with genetic predisposition to spike-wave epilepsy (WAG/Rij). Front Neurol 12: 1–6. https://doi.org/10.3389/fneur.2021.766566
  14. van Luijtelaar G, Wilde M, Citraro R, Scicchitano F, van Rijn C (2012) Does antiepileptogenesis affects sleep in genetic epileptic rats? Int J Psychophysiol 85: 49–54. https://doi.org/10.1016/j.ijpsycho.2011.09.010
  15. Kovács Z, Czurkó A, Kékesi KA, Juhász G (2012) Neonatal tricyclic antidepressant clomipramine treatment reduces the spike-wave discharge activity of the adult WAG/Rij rat. Brain Res Bull 89: 102–107. https://doi.org/10.1016/j.brainresbull.2012.07.010
  16. Mohammed HS, Khadrawy YA (2021) Electrophysiological and neurochemical evaluation of the adverse effects of REM sleep deprivation and epileptic seizures on rat’s brain. Life Sci 273: 119303. https://doi.org/10.1016/j.lfs.2021.119303
  17. Grubar JC (1983) Sleep and mental deficiency. Rev Electroencephal Neurophysiol Clin 13: 107–113. https://doi.org/10.1016/S0370-4475(83)80068-9
  18. Meeren HKM, Pijn JPM, Van Luijtelaar ELJM, Coenen AML, Da Silva FHL (2002) Cortical focus drives widespread corticothalamic networks during spontaneous absence seizures in rats. J Neurosci 22: 1480–1495. https://doi.org/10.1523/jneurosci.22-04-01480.2002
  19. Polack P-O, Guillemain I, Hu E, Deransart C, Depaulis A, Charpier S (2007) Deep layer somatosensory cortical neurons initiate spike-and-wave discharges in a genetic model of absence seizures. J Neurosci 27: 6590–6599. https://doi.org/10.1523/JNEUROSCI.0753-07.2007
  20. Lüttjohann A, Van Luijtelaar G (2012) The dynamics of cortico-thalamo-cortical interactions at the transition from pre-ictal to ictal LFPs in absence epilepsy. Neurobiol Dis 47: 49–60. https://doi.org/10.1016/j.nbd.2012.03.023
  21. Westmijse I, Ossenblok P, Gunning B, van Luijtelaar G (2009) Onset and propagation of spike and slow wave discharges in human absence epilepsy: A MEG study. Epilepsia 50: 2538–2548. https://doi.org/10.1111/j.1528-1167.2009.02162.x
  22. Sarrigiannis PG, Zhao Y, He F, Billings SA, Baster K, Rittey C, Yianni J, Zis P, Wei H, Hadjivassiliou M, Grünewald R (2018) The cortical focus in childhood absence epilepsy; evidence from nonlinear analysis of scalp EEG recordings. Clin Neurophysiol 129(3): 602–617. https://doi.org/10.1016/j.clinph.2017.11.029
  23. Fernandez LMJ, Lüthi A (2020) Sleep spindles: Mechanisms and functions. Physiol Rev 100: 805–868. https://doi.org/10.1152/physrev.00042.2018
  24. Steriade M, Deschenes M (1984) The thalamus as a neuronal oscillator. Brain Res Rev 8: 1–63. https://doi.org/10.1016/0165-0173(84)90017-1
  25. Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262(5134): 679–685. https://doi.org/10.1126/science.8235588
  26. Kostopoulos G, Gloor P, Pellegrini A, Gotman J (1981) A study of the transition from spindles to spike and wave discharge in feline generalized penicillin epilepsy: Microphysiological features. Exp Neurol 73: 55–77. https://doi.org/10.1016/0014-4886(81)90045-5
  27. Leresche N, Lambert RC, Errington AC, Crunelli V (2012) From sleep spindles of natural sleep to spike and wave discharges of typical absence seizures: Is the hypothesis still valid? Pflugers Arch 463: 201–212. https://doi.org/10.1007/s00424-011-1009-3
  28. Kozák G, Földi T, Berényi A (2020) Spike-and-wave discharges are not pathological sleep spindles, network-level aspects of age-dependent absence seizure development in rats. 7(1): eNeuro 0253-19.2019. https://doi.org/10.1523/ENEURO.0253-19.2019
  29. Sitnikova E, Hramov AE, Grubov V, Koronovsky AA (2014) Time-frequency characteristics and dynamics of sleep spindles in WAG/Rij rats with absence epilepsy. Brain Res 1543: 290–299. https://doi.org/10.1016/j.brainres.2013.11.001
  30. Gabova AV, Sarkisova KY, Fedosova EA, Shatskova AB, Morozov AA (2020) Developmental changes in peak-wave discharges in WAG/Rij rats with genetic absence epilepsy. Neurosci Behav Physiol 50: 245–252. https://doi.org/10.1007/s11055-019-00893-y
  31. Sitnikova EY, Smirnov KS, Grubov VV, Hramov AE (2019) Diagnostic principles of immature epileptic (proepileptic) EEG activity in rats with genetic predisposition to absence epilepsy. Informatsionno-Upravliaiushchie Sist 2019: 89–97. https://doi.org/10.31799/1684-8853-2019-1-89-97
  32. Sarkisova KY, Kulikov MA (2006) Behavioral characteristics of WAG/Rij rats susceptible and non-susceptible to audiogenic seizures. Behav Brain Res 166: 9–18. https://doi.org/10.1016/j.bbr.2005.07.024
  33. Surina NM, Ashapkin VV, Merzalov IB, Perepelkina OV, Fedotova IB, Pavlova GV, Poletaeva II (2014) Audiogenic seizure proneness after methyl-enriched diet in ontogeny. Dokl Biol Sci 454: 62–64. https://doi.org/10.1134/S0012496614010219
  34. Sarkisova KY, Gabova AV (2018) Maternal care exerts disease-modifying effects on genetic absence epilepsy and comorbid depression. Genes Brain Behav 17(7): e12477. https://doi.org/10.1111/gbb.12477
  35. Sarkisova KY, Gabova AV, Kulikov MA, Fedosova EA, Shatskova AB, Morosov AA (2017) Rearing by foster Wistar mother with high level of maternal care counteracts the development of genetic absence epilepsy and comorbid depression in WAG/Rij rats. Dokl Biol Sci 473: 39–42. https://doi.org/10.1134/S0012496617020077
  36. Gobbo D, Scheller A, Kirchhoff F (2021) From physiology to pathology of cortico-thalamo-cortical oscillations: astroglia as a target for further research. Front Neurol 12: 1–26. https://doi.org/10.3389/fneur.2021.661408
  37. Zhang Y, Gruber R (2019) Can slow-wave sleep enhancement improve memory? A review of current approaches and cognitive outcomes. Yale J Biol Med 92: 63–80.
  38. Fedosova EA, Shatskova AB, Sarkisova KYu (2022) Ethosuximide improves cognitive flexibility during reversal learning in WAG/Rij rats with absence epilepsy and comorbid depression. J Evol Biochem Physiol 58: 98–116. https://doi.org/10.1134/S0022093022010100
  39. Fedosova EA, Shatskova AB, Sarkisova KYu (2021) Ethosuximide increases exploratory motivation and improves episodic memory in the novel object recognition test in WAG/Rij rats with genetic absence epilepsy. Neurosci Behav Physiol 51: 501–512. https://doi.org/10.1007/s11055-021-01097-z
  40. Sarkisova K, Fedosova E, Shatskova A, Gabova A, Rudenok M, Stanishevskaya V, Slominsky P (2021) Maternal methyl-enriched diet alters absence seizures, depression-like comorbidity and DNMT1, HCN1 and TH gene expression in adult offspring. 34th Int Epilepsy Congress Virtual, 2021. Epilepsia. Special Issue. S3. 62: 135–136. https://doi.org/10.1111/epi.17079
  41. Strauss U, Kole MHP, Bräuer AU, Pahnke J, Bajorat R, Rolfs A, Nitsch R, Deisz RA (2004) An impaired neocortical Ih is associated with enhanced excitability and absence epilepsy. Eur J Neurosci 19: 3048–3058. https://doi.org/10.1111/j.0953-816X.2004.03392.x
  42. Sarkisova K, van Luijtelaar G (2022) The impact of early-life environment on absence epilepsy and neuropsychiatric comorbiidities. IBRO Neurosci Rep 13: 436–438. https://doi.org/10.1016/j.ibneur.2022.10.012
  43. Blumenfeld H, Klein JP, Schridde U, Vestal M, Rice T, Khera DS, Bashyal C, Giblin K, Paul-Laughinghouse C, Wang F, Phadke A, Mission J, Agarwal RK, Englot DJ, Motelow J, Nersesyan H, Waxman SG, Levin AR (2008) Early treatment suppresses the development of spike-wave epilepsy in a rat model. Epilepsia 49: 400–409. https://doi.org/10.1111/j.1528-1167.2007.01458.x
  44. Palagini L, Baglioni C, Ciaparelli A, Gemignani A, Riemann D (2013) REM sleep dysregulation in depression: state of the art. Sleep Med Rev 17: 377–390. https://doi.org/10.1016/j.smrv.2012.11.001
  45. Steiger A, Pawlowski M, Kimura M (2015) Sleep electroencephalography as a biomarker in depression. Chrono Physiol Ther 5: 15–25. https://doi.org/10.3390/ijms20030607

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