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Features of the EEG Pattern of Sleep Spindles and Its Diagnostic Significance in Ontogeny

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Bulletin of Experimental Biology and Medicine Aims and scope

Analysis of the microstructure of sleep using extended EEG monitoring can provide deep understanding of the neuronal activity of the brain. Sleep spindles (SS) are one of the main EEG patterns occurring during the non-rapid eye movement sleep. SS reflect the process of synchronization and provide sleep initiation and maintenance by suppressing sensory information. SS are associated with a wide range of brain functions, such as memory and neuroplasticity, general intelligence and cognitive performance, which undergo various changes throughout the life. In this review we discuss the features of the formation and regression of SS in humans during ontogeny on the basis of published data of the last 5-6 years and fundamental results of previous studies at the Scientific Centre for Family Health and Human Reproduction Problems that formed the basis of the modern study of neurophysiological phenomena of the wakefulness and sleep. The search for diagnostic patterns and prognostic markers of the pathology of higher nervous activity remains a priority in fundamental studies and medical practice. Modern methods for studying sleep and its EEG patterns are the next step in understanding the neurophysiological aspects of the sleep—wake cycle. This will open prospects for predicting postnatal maturation, understanding the mechanisms of brain neuroplasticity in the “sleep—wakefulness” continuum, which is one of the tasks of modern somnology and neurophysiology.

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References

  1. Berdina ON, Rychkova LV, Madaeva IM. Characteristics of sleep structure in schoolchildren with high intellectual abilities. Zh. Nevrol. Psikhiatr. 2018;118(7):78-81. Russian. doi: 10.17116/jnevro20181187178

  2. Kolesnikov SI, Kolesnikova LI. Development of brain electrogenesis in children aged 1 to 7 years. Brain: Theoretical and Clinical Aspects. Pokrovsky VI, ed. Moscow, 2003. P. 193-241. Russian.

  3. Korolyeva NV, Gutnik IN, Kolesnikov SI. Fundamentals of Clinical Electroencephalography. Irkutsk, 2005. Russian.

  4. Korolyeva NV, Kolesnikov SI. Formation of Children’s Brain Bioelectric Activity in Ontogeny. Irkutsk, 2005. Russian.

  5. Koroleva NV, Kolesnikov SI, Vorob’ev SV. Electroencephalographic Atlas of Epilepsies and Epileptic Syndromes in Children. Moscow, 2011. Russian.

  6. Korolyova NV, Kolesnikov SI, Dolgih VV. Correlation between electroencephalographic parameters in children depending on the electroencephalogram type. Ultrazvuk. Funktsional. Diagnost. 2001;(2):122-132. Russian.

    Google Scholar 

  7. Koshchavtsev AG, Grechanyi SV. Interpretation of electroencephalography in infants. Epilepsiya Paroksizm. Sostoyaniya. 2020;12(1):9-25. Russian. doi: 10.17749/2077-8333.2020.12.1.9-25

  8. Madaeva IM, Shevyrtalova ON, Dolgich VV. Arterial hypertension and sleep apnea in pediatrics: results of pilot trial. Pediatriya. Consilium Medicum. 2009;(3):114-116. Russian.

    Google Scholar 

  9. Melashenko TV, Guzeva VV. Particular transit patterns EEG in premature babies with hypoxia-ischemic encephalopathy. Pediatr. 2014;5(1):32-36. Russian.

    Google Scholar 

  10. Petrukhin AS, Sozaeva NS, Golosnaya GS. Neurobiologic and ontogenetic basis of motor functions development. Russ. Zh. Det. Nevrol. 2009;4(2):20-23. Russian.

    Google Scholar 

  11. Polyakov VM, Kolesnikova LI, Kolesnikov SI, Dolgikh VV, Kosovtseva AS, Rychkova LV, Prokhorova ZV. Peculiarities of functional hemispheric asymmetry formation in children and adolescents with hypertension. Vestn. Ross. Acad. Med. Nauk. 2014;69(9-10):77-82. Russian. doi: 10.15690/vramn.v69i9-10.1135

  12. Shevyrtalova ON, Protopopova ON, Madayeva IM, Dolgikh VV, Kolesnikova LI, Polyakov VM, Prokhorova ZhV. Sleep disorders in the genesis of emotional personality and cognitive disorders in adolescents with essential hypertension. Ross. Pediatr. Zh. 2011;(2):12-16. Russian.

    Google Scholar 

  13. Aeschbach D, Borbély AA. All-night dynamics of the human sleep EEG. J. Sleep Res. 1993;2(2):70-81. doi: https://doi.org/10.1111/j.1365-2869.1993.tb00065.x

    Article  CAS  PubMed  Google Scholar 

  14. Ambrosius U, Lietzenmaier S, Wehrle R, Wichniak A, Kalus S, Winkelmann J, Bettecken T, Holsboer F, Yassouridis A, Friess E. Heritability of sleep electroencephalogram. Biol. Psychiatry. 2008;64(4):344-348. doi: https://doi.org/10.1016/j.biopsych.2008.03.002

    Article  PubMed  Google Scholar 

  15. Anderson CM, Torres F, Faoro A. The EEG of the early premature. Electroencephalogr. Clin. Neurophysiol. 1985;60(2):95-105. doi: https://doi.org/10.1016/0013-4694(85)90015-x

    Article  CAS  PubMed  Google Scholar 

  16. André M, Lamblin MD, d’Allest AM, Curzi-Dascalova L, Moussalli-Salefranque F, S Nguyen The T, Vecchierini-Blineau MF, Wallois F, Walls-Esquivel E, Plouin P. Electroencephalography in premature and full-term infants. Developmental features and glossary. Neurophysiol. Clin. 2010;40(2):59-124. doi: https://doi.org/10.1016/j.neucli.2010.02.002

  17. Andrillon T, Nir Y, Staba RJ, Ferrarelli F, Cirelli C, Tononi G, Fried I. Sleep spindles in humans: insights from intracranial EEG and unit recordings. J. Neurosci. 2011;31(49):17 821-17 834. doi: 10.1523/JNEUROSCI.2604-11.2011

  18. Antony JW, Schönauer M, Staresina BP, Cairney SA. Sleep spindles and memory reprocessing. Trends Neurosci. 2019;42(1):1-3. doi: https://doi.org/10.1016/j.tins.2018.09.012

    Article  CAS  PubMed  Google Scholar 

  19. Ayoub A, Aumann D, Hörschelmann A, Kouchekmanesch A, Paul P, Born J, Marshall L. Differential effects on fast and slow spindle activity, and the sleep slow oscillation in humans with carbamazepine and flunarizine to antagonize voltage-dependent Na+ and Ca2+ channel activity. Sleep. 2013;36(6):905-911. doi: https://doi.org/10.5665/sleep.2722

    Article  PubMed  PubMed Central  Google Scholar 

  20. Berdina O, Madaeva I, Bolshakova S, Tsykunova M, Bugun O, Rychkova L. Applying a translated version of the adolescent sleep habits survey in Russian high school children with obesity. Int. J. Biomed. 2020;10(1):61-65. doi: https://doi.org/10.21103/Article10(1)_OA10

    Article  Google Scholar 

  21. Berry RB, Budhiraja R, Gottlieb DJ, Gozal D, Iber C, Kapur VK, Marcus CL, Mehra R, Parthasarathy S, Quan SF, Redline S, Strohl KP, Davidson Ward SL, Tangredi MM; American Academy of Sleep Medicine. Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine. J. Clin. Sleep Med. 2012;8(5):597-619. doi: https://doi.org/10.5664/jcsm.2172

    Article  PubMed  PubMed Central  Google Scholar 

  22. Boylan G, Murray D, Rennie J. The normal EEG and aEEG. Neonatal Cerebral Investigation. Rennie J, Hagmann C, Robertson N, eds. Cambridge, 2008. P. 83-91. doi:https://doi.org/10.1017/CBO9780511544750.008

  23. Campbell IG, Feinberg I. Maturational patterns of sigma frequency power across childhood and adolescence: a longitudinal study. Sleep. 2016;39(1):193-201. doi: https://doi.org/10.5665/sleep.5346

    Article  PubMed  PubMed Central  Google Scholar 

  24. Cardozo PL, de Lima IBQ, Maciel EMA, Silva NC, Dobransky T, Ribeiro FM. Synaptic elimination in neurological disorders. Curr. Neuropharmacol. 2019;17(11):1071-1095. doi: https://doi.org/10.2174/1570159X17666190603170511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Clawson BC, Durkin J, Aton SJ. Form and function of sleep spindles across the lifespan. Neural. Plast. 2016;2016:6936381. doi: https://doi.org/10.1155/2016/6936381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Counsell SJ, Maalouf EF, Fletcher AM, Duggan P, Battin M, Lewis HJ, Herlihy AH, Edwards AD, Bydder GM, Rutherford MA. MR imaging assessment of myelination in the very preterm brain. AJNR Am. J. Neuroradiol. 2002;23(5):872-881.

    PubMed  PubMed Central  Google Scholar 

  27. Cox R, Schapiro AC, Manoach DS, Stickgold R. Individual differences in frequency and topography of slow and fast sleep spindles. Front. Hum. Neurosci. 2017;11:433. doi: https://doi.org/10.3389/fnhum.2017.00433

    Article  PubMed  PubMed Central  Google Scholar 

  28. Crowley K, Trinder J, Kim Y, Carrington M, Colrain IM. The effects of normal aging on sleep spindle and K-complex production. Clin. Neurophysiol. 2002;113(10)1615-1622. doi: https://doi.org/10.1016/s1388-2457(02)00237-7

    Article  PubMed  Google Scholar 

  29. D’Atri A, Novelli L, Ferrara M, Bruni O, De Gennaro L. Different maturational changes of fast and slow sleep spindles in the first four years of life. Sleep Med. 2018;42:73-82. doi: https://doi.org/10.1016/j.sleep.2017.11.1138

    Article  PubMed  Google Scholar 

  30. De Gennaro L, Ferrara M. Sleep spindles: an overview. Sleep Med. Rev. 2003;7(5):423-440. doi: https://doi.org/10.1053/smrv.2002.0252

    Article  PubMed  Google Scholar 

  31. Destexhe A, Contreras D, Steriade M. Cortically-induced coherence of a thalamic-generated oscillation. Neuroscience. 1999;92(2):427-443. doi: https://doi.org/10.1016/s0306-4522(99)00024-x

    Article  CAS  PubMed  Google Scholar 

  32. Ellingson RJ. Development of sleep spindle bursts during the first year of life. Sleep. 1982;5(1):39-46.

    Article  CAS  Google Scholar 

  33. Ellingson RJ, Peters JF. Development of EEG and daytime sleep patterns in Trisomy-21 infants during the first year of life: longitudinal observations. Electroencephalogr. Clin. Neurophysiol. 1980;50(5-6):457-466. doi: https://doi.org/10.1016/0013-4694(80)90012-7

    Article  CAS  PubMed  Google Scholar 

  34. Feinberg I. Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? J. Psychiatr. Res. 1982-1983;17(4):319-334. doi: https://doi.org/10.1016/0022-3956(82)90038-3

  35. Feinberg I, Campbell IG. Sleep EEG changes during adolescence: an index of a fundamental brain reorganization. Brain Cogn. 2010;72(1):56-65. doi: https://doi.org/10.1016/j.bandc.2009.09.008

    Article  PubMed  Google Scholar 

  36. Feinberg I, Campbell IG. Longitudinal sleep EEG trajectories indicate complex patterns of adolescent brain maturation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2013;304(4):R296-R303. doi: https://doi.org/10.1152/ajpregu.00422.2012

    Article  CAS  PubMed  Google Scholar 

  37. Fernandez LMJ, Lüthi A. Sleep spindles: mechanisms and functions. Physiol. Rev. 2020;100(2):805-868. doi: https://doi.org/10.1152/physrev.00042.2018

    Article  PubMed  Google Scholar 

  38. Fjell AM, Westlye LT, Amlien I, Espeseth T, Reinvang I, Raz N, Agartz I, Salat DH, Greve DN, Fischl B, Dale AM, Walhovd KB. High consistency of regional cortical thinning in aging across multiple samples. Cereb. Cortex. 2009;19(9):2001-2012. doi: https://doi.org/10.1093/cercor/bhn232

    Article  PubMed  PubMed Central  Google Scholar 

  39. Goldstone A, Willoughby AR, de Zambotti M, Clark DB, Sullivan EV, Hasler BP, Franzen PL, Prouty DE, Colrain IM, Baker FC. Sleep spindle characteristics in adolescents. Clin. Neurophysiol. 2019;130(6):893-902. doi: https://doi.org/10.1016/j.clinph.2019.02.019

    Article  PubMed  PubMed Central  Google Scholar 

  40. Goldstone A, Willoughby AR, de Zambotti M, Franzen PL, Kwon D, Pohl KM, Pfefferbaum A, Sullivan EV, Müller-Oehring EM, Prouty DE, Hasler BP, Clark DB, Colrain IM, Baker FC. The mediating role of cortical thickness and gray matter volume on sleep slow-wave activity during adolescence. Brain Struct. Funct. 2018;223(2):669-685. doi: https://doi.org/10.1007/s00429-017-1509-9

    Article  PubMed  Google Scholar 

  41. Gorgoni M, Lauri G, Truglia I, Cordone S, Sarasso S, Scarpelli S, Mangiaruga A, D’Atri A, Tempesta D, Ferrara M, Marra C, Rossini PM, De Gennaro L. Parietal fast sleep spindle density decrease in Alzheimer’s disease and amnesic mild cognitive impairment. Neural Plast. 2016;2016:8376108. doi: https://doi.org/10.1155/2016/8376108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Gruber R, Wise MS, Frenette S, Knäauper B, Boom A, Fontil L, Carrier J. The association between sleep spindles and IQ in healthy school-age children. Int. J. Psychophysiol. 2013;89(2):229-240. doi: https://doi.org/10.1016/j.ijpsycho.2013.03.018

    Article  PubMed  Google Scholar 

  43. Gunn DG, Naismith SL, Terpening Z, Lewis SJ. The relationships between poor sleep efficiency and mild cognitive impairment in Parkinson disease. J. Geriatr. Psychiatry Neurol. 2014;27(2):77-84. doi: https://doi.org/10.1177/0891988713509135

    Article  PubMed  Google Scholar 

  44. Hagne I. Development of the EEG in normal infants during the first year of life. A longitudinal study. Acta Paediatr. Scand. Suppl. 1972;232:1-53.

    CAS  PubMed  Google Scholar 

  45. Hata Y. Synaptic Elimination. Encyclopedia of Neuroscience. Binder MD, Hirokawa N, Windhorst U, eds. Berlin, 2009.

  46. Holz J, Piosczyk H, Feige B, Spiegelhalder K, Baglioni C, Riemann D, Nissen C. EEG Σ and slow-wave activity during NREM sleep correlate with overnight declarative and procedural memory consolidation. J. Sleep Res. 2012;21(6):612-619. doi: https://doi.org/10.1111/j.1365-2869.2012.01017.x

    Article  PubMed  Google Scholar 

  47. Jankel WR, Niedermeyer E. Sleep spindles. J. Clin. Neurophysiol. 1985;2(1):1-35. doi: https://doi.org/10.1097/00004691-198501000-00001

    Article  CAS  PubMed  Google Scholar 

  48. Kaminska A, Eisermann M, Plouin P. Child EEG (and maturation). Handb. Clin. Neurol. 2019;160:125-142. doi: https://doi.org/10.1016/B978-0-444-64032-1.00008-4

    Article  CAS  PubMed  Google Scholar 

  49. Khazipov R, Luhmann HJ. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 2006;29(7):414-418. doi: https://doi.org/10.1016/j.tins.2006.05.007

    Article  CAS  PubMed  Google Scholar 

  50. Knickmeyer RC, Gouttard S, Kang C, Evans D, Wilber K, Smith JK, Hamer RM, Lin W, Gerig G, Gilmore JH. A structural MRI study of human brain development from birth to 2 years. J. Neurosci. 2008;28(47):12 176-12 182. doi: 10.1523/JNEUROSCI.3479-08.2008

  51. Koszer SE, Moshé SL, Holmes GL. Visual analysis of the neonatal electroencephalogram. Clinical Neurophysiology of Infancy, Childhood, and Adolescence. Elsevier, 2006. P. 70-86.

  52. Landolt HP. Genetic determination of sleep EEG profiles in healthy humans. Prog. Brain Res. 2011;193:51-61. doi: https://doi.org/10.1016/B978-0-444-53839-0.00004-1

    Article  PubMed  Google Scholar 

  53. Latreille V, Carrier J, Lafortune M, Postuma RB, Bertrand JA, Panisset M, Chouinard S, Gagnon JF. Sleep spindles in Parkinson’s disease may predict the development of dementia. Neurobiol. Aging. 2015;36(2):1083-1090. doi: https://doi.org/10.1016/j.neurobiolaging.2014.09.009

    Article  PubMed  Google Scholar 

  54. Leger D, Beck F, Richard JB, Godeau E. Total sleep time severely drops during adolescence. PLoS One. 2012;7(10):e45204. doi: https://doi.org/10.1371/journal.pone.0045204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Liu S, Pan J, Tang K, Lei Q, He L, Meng Y, Cai X, Li Z. Sleep spindles, K-complexes, limb movements and sleep stage proportions may be biomarkers for amnestic mild cognitive impairment and Alzheimer’s disease. Sleep Breath. 2020;24(2):637-651. doi: https://doi.org/10.1007/s11325-019-01970-9

    Article  PubMed  Google Scholar 

  56. Loomis AL, Harvey EN, Hobart G. Potential rhythms of the cerebral cortex during sleep. Science. 1935;81:597-598. doi: https://doi.org/10.1126/science.81.2111.597

    Article  CAS  PubMed  Google Scholar 

  57. Lüthi A. Sleep spindles: where they come from, what they do. Neuroscientist. 2014;20(3):243-256. doi: https://doi.org/10.1177/1073858413500854

    Article  PubMed  Google Scholar 

  58. Madaeva I, Shevyrtalova O, Dolgikh V, Kolesnikova L. Obstructive sleep apnea/hypopnea syndrome in adolescents with essential hypertension. Sleep Med. 2009;10(10):1167-1168. doi: https://doi.org/10.1016/j.sleep.2009.04.002

    Article  PubMed  Google Scholar 

  59. Mak-McCully RA, Rolland M, Sargsyan A, Gonzalez C, Magnin M, Chauvel P, Rey M, Bastuji H, Halgren E. Coordination of cortical and thalamic activity during non-REM sleep in humans. Nat. Commun. 2017;8:15499. doi: https://doi.org/10.1038/ncomms15499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Mander BA, Winer JR, Walker MP. Sleep and human aging. Neuron. 2017;94(1):19-36. doi: https://doi.org/10.1016/j.neuron.2017.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Martin N, Lafortune M, Godbout J, Barakat M, Robillard R, Poirier G, Bastien C, Carrier J. Topography of age-related changes in sleep spindles. Neurobiol. Aging. 2013;34(2):468-476. doi: https://doi.org/10.1016/j.neurobiolaging.2012.05.020

    Article  PubMed  Google Scholar 

  62. Milh M, Kaminska A, Huon C, Lapillonne A, Ben-Ari Y, Khazipov R. Rapid cortical oscillations and early motor activity in premature human neonate. Cereb. Cortex. 2007;17(7):1582-1594. doi: https://doi.org/10.1093/cercor/bhl069

    Article  PubMed  Google Scholar 

  63. Nelson PT, Abner EL, Scheff SW, Schmitt FA, Kryscio RJ, Jicha GA, Smith CD, Patel E, Markesbery WR. Alzheimer’s-type neuropathology in the precuneus is not increased relative to other areas of neocortex across a range of cognitive impairment. Neurosci. Lett. 2009;450(3):336-339. doi: https://doi.org/10.1016/j.neulet.2008.11.006

    Article  CAS  PubMed  Google Scholar 

  64. Nicolas A, Petit D, Rompré S, Montplaisir J. Sleep spindle characteristics in healthy subjects of different age groups. Clin. Neurophysiol. 2001;112(3):521-527. doi: https://doi.org/10.1016/s1388-2457(00)00556-3

    Article  CAS  PubMed  Google Scholar 

  65. Northcutt RG. Body and Brain. A Trophic Theory of Neural Connections. Dale Purves. Harvard University Press, Cambridge, MA, 1988. viii, 231 pp., illus. $35. Science. 1989;244:993. doi: 10.1126/science.244.4907.993

  66. Peter-Derex L, Comte JC, Mauguière F, Salin PA. Density and frequency caudo-rostral gradients of sleep spindles recorded in the human cortex. Sleep. 2012;35(1):69-79. doi: https://doi.org/10.5665/sleep.1588

    Article  PubMed  PubMed Central  Google Scholar 

  67. Picard-Deland C, Carr M, Paquette T, Saint-Onge K, Nielsen T. Sleep spindle and psychopathology characteristics of frequent nightmare recallers. Sleep Med. 2018;50:113-131. doi: https://doi.org/10.1016/j.sleep.2017.10.003

    Article  PubMed  Google Scholar 

  68. Purcell SM, Manoach DS, Demanuele C, Cade BE, Mariani S, Cox R, Panagiotaropoulou G, Saxena R, Pan JQ, Smoller JW, Redline S, Stickgold R. Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource. Nat. Commun. 2017;8:15930. doi: https://doi.org/10.1038/ncomms15930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Rauchs G, Schabus M, Parapatics S, Bertran F, Clochon P, Hot P, Denise P, Desgranges B, Eustache F, Gruber G, Anderer P. Is there a link between sleep changes and memory in Alzheimer’s disease? Neuroreport. 2008;19(11):1159-1162. doi: https://doi.org/10.1097/WNR.0b013e32830867c4

    Article  PubMed  PubMed Central  Google Scholar 

  70. Reichert CF, Veitz S, Bühler M, Gruber G, Deuring G, Rehm SS, Rentsch K, Garbazza C, Meyer M, Slawik H, Lin YS, Weibel J. Wide awake at bedtime? Effects of caffeine on sleep and circadian timing in male adolescents — a randomized crossover trial. Biochem. Pharmacol. 2021;191:114283. doi: https://doi.org/10.1016/j.bcp.2020.114283

    Article  CAS  PubMed  Google Scholar 

  71. Reynolds CM, Gradisar M, Coussens S, Short MA. Sleep spindles in adolescence: a comparison across sleep restriction and sleep extension. Sleep Med. 2018;50:166-174. doi: https://doi.org/10.1016/j.sleep.2018.05.019

    Article  PubMed  Google Scholar 

  72. Rychkova L, Madaeva I, Berdina O, Bolshakova S, Bugun O. 211 Inadequate sleep habits ARE associated with obesity in high school children. Arch. Dis. Childhood. 2021;106:A89. doi: https://doi.org/10.1136/archdischild-2021-europaediatrics.211

    Article  Google Scholar 

  73. Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, Darsaud A, Degueldre C, Desseilles M, Gais S, Phillips C, Rauchs G, Schnakers C, Sterpenich V, Vandewalle G, Luxen A, Maquet P. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl Acad. Sci. USA. 2007;104(32):13164-13169. doi: https://doi.org/10.1073/pnas.0703084104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Scholle S, Zwacka G, Scholle HC. Sleep spindle evolution from infancy to adolescence. Clin. Neurophysiol. 2007;118(7):1525-1531. doi: https://doi.org/10.1016/j.clinph.2007.03.007

    Article  CAS  PubMed  Google Scholar 

  75. Seibt J, Timofeev I, Carrier J, Peyrache A. Role of spindle oscillations across lifespan in health and disease. Neural Plast. 2016;2016:8103439. doi: https://doi.org/10.1155/2016/8103439

    Article  PubMed  PubMed Central  Google Scholar 

  76. Shinomiya S, Nagata K, Takahashi K, Masumura T. Development of sleep spindles in young children and adolescents. Clin. Electroencephalogr. 1999;30(2):39-43. doi: https://doi.org/10.1177/155005949903000203

    Article  CAS  PubMed  Google Scholar 

  77. Skeldon AC, Derks G, Dijk DJ. Modelling changes in sleep timing and duration across the lifespan: Changes in circadian rhythmicity or sleep homeostasis? Sleep Med. Rev. 2016;28:96-107. doi: https://doi.org/10.1016/j.smrv.2015.05.011

    Article  PubMed  Google Scholar 

  78. Steriade M, Timofeev I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron. 2003;37(4):563-576. doi: https://doi.org/10.1016/s0896-6273(03)00065-5

    Article  CAS  PubMed  Google Scholar 

  79. Tarokh L, Carskadon MA. Developmental changes in the human sleep EEG during early adolescence. Sleep. 2010;33(6):801-809. doi: https://doi.org/10.1093/sleep/33.6.801

    Article  PubMed  PubMed Central  Google Scholar 

  80. Tau GZ, Peterson BS. Normal development of brain circuits. Neuropsychopharmacology. 2010;35(1):147-168. doi: https://doi.org/10.1038/npp.2009.115

    Article  PubMed  Google Scholar 

  81. Tsuchida TN, Wusthoff CJ, Shellhaas RA, Abend NS, Hahn CD, Sullivan JE, Nguyen S, Weinstein S, Scher MS, Riviello JJ, Clancy RR; American Clinical Neurophysiology Society Critical Care Monitoring Committee. American clinical neurophysiology society standardized EEG terminology and categorization for the description of continuous EEG monitoring in neonates: report of the American Clinical Neurophysiology Society critical care monitoring committee. J. Clin. Neurophysiol. 2013;30(2):161-173. doi: https://doi.org/10.1097/WNP.0b013e3182872b24

    Article  PubMed  Google Scholar 

  82. Volpe JJ. Specialized studies in the neurological evaluation. Neurology of the Newborn. Philadelphia, 2008. P. 154-202.

  83. Warby SC, Wendt SL, Welinder P, Munk EG, Carrillo O, Sorensen HB, Jennum P, Peppard PE, Perona P, Mignot E. Sleep-spindle detection: crowdsourcing and evaluating performance of experts, non-experts and automated methods. Nat. Methods. 2014;11(4):385-392. doi: https://doi.org/10.1038/nmeth.2855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Weaver E, Gradisar M, Dohnt H, Lovato N, Douglas P. The effect of presleep video-game playing on adolescent sleep. J. Clin. Sleep Med. 2010;6(2):184-189.

    Article  Google Scholar 

  85. Westlye LT, Walhovd KB, Dale AM, Bjørnerud A, Due-Tønnessen P, Engvig A, Grydeland H, Tamnes CK, Østby Y, Fjell AM. Differentiating maturational and aging-related changes of the cerebral cortex by use of thickness and signal intensity. Neuroimage. 2010;52(1):172-185. doi: https://doi.org/10.1016/j.neuroimage.2010.03.056

    Article  PubMed  Google Scholar 

  86. Whitehead K, Pressler R, Fabrizi L. Characteristics and clinical significance of delta brushes in the EEG of premature infants. Clin. Neurophysiol. Pract. 2016;2:12-18. doi: https://doi.org/10.1016/j.cnp.2016.11.002

    Article  PubMed  PubMed Central  Google Scholar 

  87. Whitelaw BS. Microglia-mediated synaptic elimination in neuronal development and disease. J. Neurophysiol. 2018;119(1):1-4. doi: https://doi.org/10.1152/jn.00021.2017

    Article  CAS  PubMed  Google Scholar 

  88. Zhang ZY, Campbell IG, Dhayagude P, Espino HC, Feinberg I. Longitudinal analysis of sleep spindle maturation from childhood through late adolescence. J. Neurosci. 2021;41(19):4253-4261. doi: https://doi.org/10.1523/JNEUROSCI.2370-20.2021

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to E. B. Ukhinov.

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Translated from Byulleten’ Eksperimental’noi Biologii i Meditsiny, Vol. 173, No. 4, pp. 404-415, April, 2022

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Ukhinov, E.B., Madaeva, I.M., Berdina, O.N. et al. Features of the EEG Pattern of Sleep Spindles and Its Diagnostic Significance in Ontogeny. Bull Exp Biol Med 173, 399–408 (2022). https://doi.org/10.1007/s10517-022-05557-5

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